Teratozoospermia: Spotlight on the main genetic actors in the human

Human Reproduction Update

Volumn 21, Issue 4, 2014, Pages 455-485

  Coutton, Charles ^a,b,c   Escoffier, Jessica ^a,b,d   Martinez, Guillaume ^a,b   Arnoult, Christophe ^a,b   Ray, Pierre F ^a,b,e  

^a UNIV GRENOBLE ALPES   (France)

^b INSTITUT ALBERT BONNIOT   (France)

^c UF de Génétique Chromosomique   (France)

^d UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^e GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Gene mutations; Genetic diagnosis; Male infertility; Sperm morphology; Teratozoospermia

Indexed keywords

AURORA C KINASE; CALCIUM IONOPHORE; DYNEIN ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PROTEIN DPY19L2; UNCLASSIFIED DRUG; DNAH1 PROTEIN, HUMAN; DPY19L2 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; SPATA16 PROTEIN, HUMAN;

ANEUPLOIDY; ARTICLE; ARTIFICIAL OOCYTE ACTIVATION; AURKC GENE; CILIARY DYSKINESIA; COPY NUMBER VARIATION; DNAH1 GENE; DPY19L2 GENE; ENZYME ACTIVITY; EUKARYOTIC FLAGELLUM; FERTILIZATION IN VITRO; GENE; GENE DELETION; GENE MUTATION; GENE THERAPY; GLOBOZOOSPERMIA; HOMOZYGOSITY; HUMAN; HUMAN GENETICS; INFERTILITY THERAPY; INTRACYTOPLASMIC SPERM INJECTION; LARGE HEADED MULTIFLAGELLAR SPERMATOZOA; MALE INFERTILITY; MEIOSIS; MICROTUBULE; MULTIPLE MORPHOLOGICAL ABNORMALITY OF THE FLAGELLA; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPIC VARIATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEGMENTAL DUPLICATION; SPERMATOZOON ABNORMALITY; SYSTEMATIC REVIEW; ALLELE; ANIMAL; CONGENITAL MALFORMATION; CYTOLOGY; GENETICS; MALE; METABOLISM; POINT MUTATION; SPERMATOGENESIS; SPERMATOZOON;

ALLELES; ANIMALS; AURORA KINASE C; DYNEINS; HOMEODOMAIN PROTEINS; HUMANS; INFERTILITY, MALE; MALE; MEMBRANE PROTEINS; POINT MUTATION; SPERMATOGENESIS; SPERMATOZOA;

EID: 84938515086     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmv020     Document Type: Article

References (301)

1. Achard V, Paulmyer-Lacroix O, Mercier G, Porcu G, Saias-Magnan J, Metzler-Guillemain C, Guichaoua MR. Reproductive failure in patients with various percentages of macronuclear spermatozoa: high level of aneuploid and polyploid spermatozoa. J Androl 2007;28:600-606.
2. Afzelius BA, Eliasson R. Male and female infertility problems in the immotile-cilia syndrome. Eur J Respir Dis Suppl 1983;127:144-147.
3. Alvarez Sedó C, Rawe VY, Chemes HE. Acrosomal biogenesis in human globozoospermia: immunocytochemical, ultrastructural and proteomic studies. Hum Reprod 2012;27:1912-1921.
4. Amdani SN, Jones C, Coward K. Phospholipase C zeta (PLCz): oocyte activation and clinical links to male factor infertility. Adv Biol Regul 2013;53:292-308.
5. Anton-Lamprecht I, Kotzur B, Schopf E. Round-headed human spermatozoa. Fertil Steril 1976;27:685-693.
6. Antony D, Becker-Heck A, Zariwala MA, Schmidts M, Onoufriadis A, Forouhan M, Wilson R, Taylor-Cox T, Dewar A, Jackson C et al. Mutations in CCDC39 and CCDC40 are the major cause of primary ciliary dyskinesia with axonemal disorganization and absent inner dynein arms. Hum Mutat 2013;34:462-472.
7. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus-oocyte complex gene-expression profile. Hum Reprod 2006;21:1705-1719.
8. Audouard C, Christians E. Hsp90b1 knockout targeted to male germline: a mouse model for globozoospermia. Fertil Steril 2011;95:1475-1477.e1-4.
9. Austin-Tse C, Halbritter J, Zariwala MA, Gilberti RM, Gee HY, Hellman N, Pathak N, Liu Y, Panizzi JR, Patel-King RS et al. Zebrafish ciliopathy screen plus human mutational analysis identifies C21orf59 and CCDC65 defects as causing primary ciliary dyskinesia. Am J Hum Genet 2013;93:672-686.
10. Avo Santos M, van de Werken C, de Vries M, Jahr H, Vromans MJM, Laven JSE, Fauser BC, Kops GJ, Lens SM, Baart EB. A role for Aurora C in the chromosomal passenger complex during human preimplantation embryo development. Hum Reprod 2011;26:1868-1881.
11. 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;25:331-335.
12. 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;82:463-468.
13. 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 2005a; 20:2790-2794.
14. 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 2005b;84:123-129.
15. Baker MA, Naumovski N, Hetherington L, Weinberg A, Velkov T, Aitken RJ. Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 2013;13:61-74.
16. Balboula AZ, Schindler K. Selective disruption of aurora C kinase reveals distinct functions from aurora B kinase during meiosis in mouse oocytes. PLoS Genet 2014; 10:e1004194.
17. Bartoloni L, Blouin J-L, Pan Y, Gehrig C, Maiti AK, Scamuffa N, Rossier C, Jorissen M, Armengot M, Meeks M 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;99:10282-10286.
18. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 2010;327:836-840.
19. Becker M, Stolz A, Ertych N, Bastians H. Centromere localization of INCENP-Aurora B is sufficient to support spindle checkpoint function. Cell Cycle Georget Tex 2010; 9:1360-1372.
20. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, Sullivan-Brown J, McSheene J, Loges NT, Olbrich H, Haeffner K et al. The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 2011;43:79-84.
21. Ben Khelifa M, Zouari R, Harbuz R, Halouani L, Arnoult C, Lunardi J, Ray PF. A new AURKC mutation causing macrozoospermia: implications for human spermatogenesis and clinical diagnosis. Mol Hum Reprod 2011;17:762-768.
22. Ben Khelifa M, Coutton C, Blum MGB, Abada F, Harbuz R, Zouari R, Guichet A, May-Panloup P, Mitchell V, Rollet J et al. Identification of a new recurrent aurora kinase C mutation in both European and African men with macrozoospermia. Hum Reprod 2012;27:3337-3346.
23. Ben Khelifa M, Coutton C, Zouari R, Karaouzène T, Rendu J, Bidart M, Yassine S, Pierre V, Delaroche J, Hennebicq S 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; 94:95-104.
24. Benzacken B, Gavelle FM, Martin-Pont B, Dupuy O, Lièvre N, Hugues JN, Wolf JP. Familial sperm polyploidy induced by genetic spermatogenesis failure: case report. Hum Reprod 2001;16:2646-2651.
25. Bernard M, Sanseau P, Henry C, Couturier A, Prigent C. Cloning of STK13, a third human protein kinase related to Drosophila aurora and budding yeast Ipl1 that maps on chromosome 19q13.3-ter. Genomics 1998;53:406-409.
26. Bettencourt-Dias M, Glover DM. Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 2007;8:451-463.
27. Bisgrove BW, Yost HJ. The roles of cilia in developmental disorders and disease. Development 2006;133:4131-4143.
28. Blanchard Y, Lescoat D, Le Lannou D. Anomalous distribution of nuclear basic proteins in round-headed human spermatozoa. Andrologia 1990;22:549-555.
29. Blanchon S, Legendre M, Copin B, Duquesnoy P, Montantin G, Kott E, Dastot F, Jeanson L, Cachanado M, Rousseau A et al. Delineation of CCDC39/CCDC40 mutation spectrum and associated phenotypes in primary ciliary dyskinesia. J Med Genet 2012;49:410-416.
30. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 2007;22:1506-1512.
31. Boon M, Jorissen M, Proesmans M, De Boeck K. Primary ciliary dyskinesia, an orphan disease. Eur J Pediatr 2013;172:151-162.
32. Brahem S, Mehdi M, Elghezal H, Saad A. Analysis of sperm aneuploidies and DNA fragmentation in patients with globozoospermia or with abnormal acrosomes. Urology 2011;77:1343-1348.
33. Brahem S, Mehdi M, Elghezal H, Saad A. Study of aneuploidy rate and sperm DNA fragmentation in large-headed, multiple-tailed spermatozoa. Andrologia 2012; 44:130-135.
34. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974;77:71-94.
35. Brown PR, Miki K, Harper DB, Eddy EM. A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biol Reprod 2003;68:2241-2248.
36. Brown JR, Koretke KK, Birkeland ML, Sanseau P, Patrick DR. Evolutionary relationships of Aurora kinases: implications for model organism studies and the development of anti-cancer drugs. BMC Evol Biol 2004;4:39.
37. Brugo-Olmedo S, Chillik C, Kopelman S. Definition and causes of infertility. Reprod Biomed Online 2001;2:41-53.
38. Buettner FFR, Ashikov A, Tiemann B, Lehle L, Bakker H. C. elegans DPY-19 is a C-mannosyltransferase glycosylating thrombospondin repeats. Mol Cell 2013; 50:295-302.
39. Bui KH, Sakakibara H, Movassagh T, Oiwa K, Ishikawa T. Molecular architectureof inner dynein arms in situ in Chlamydomonas reinhardtii flagella. J Cell Biol 2008; 183:923-932.
40. Bukowy-Bieryłło Z, Ziętkiewicz E, Loges NT, Wittmer M, Geremek M, Olbrich H, Fliegauf M, Voelkel K, Rutkiewicz E, Rutland J et al. RPGR mutations might cause reduced orientation of respiratory cilia. Pediatr Pulmonol 2013;48:352-363.
41. Campbell PK, Waymire KG, Heier RL, Sharer C, Day DE, Reimann H, Jaje JM, Friedrich GA, Burmeister M, Bartness TJ et al. Mutation of a novel gene results in abnormal development of spermatid flagella, loss of intermale aggression and reduced body fat in mice. Genetics 2002;162:307.
42. Carmena M, Earnshaw WC. The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 2003;4:842-854.
43. Carmena M, Wheelock M, Funabiki H, Earnshaw WC. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 2012;13:789-803.
44. Carrell DT, Emery BR, Liu L. Characterization of aneuploidy rates, protamine levels, ultrastructure, and functional ability of round-headed sperm from two siblings and implications for intracytoplasmic sperm injection. Fertil Steril 1999; 71:511-516.
45. Carson AR, Cheung J, Scherer SW. Duplication and relocation of the functional DPY19L2 gene within low copy repeats. BMC Genomics 2006;7:45.
46. Castleman VH, Romio L, Chodhari R, Hirst RA, de Castro SCP, Parker KA, Ybot-Gonzalez P, Emes RD, Wilson SW, Wallis C et al. Mutations in radial spoke head protein genes RSPH9 and RSPH4A cause primary ciliary dyskinesia with central-microtubular-pair abnormalities. Am J Hum Genet 2009;84:197-209.
47. Chan CS, Botstein D. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 1993;135:677-691.
48. Chelli MH, Albert M, Ray PF, Guthauser B, Izard V, Hammoud I, Selva J, Vialard F. Can intracytoplasmic morphologically selected sperm injection be used to select normal-sized sperm heads in infertile patients with macrocephalic sperm head syndrome? Fertil Steril 2010;93:1347.e1-5.
49. Chemes HE. Sperm centrioles and their dual role in flagellogenesis and cell cycle of the zygote. In: Schatten H. (ed) The Centrosome. Humana Press, 2012, 33-48. Available at: http://link.springer.com.gate2.inist.fr/chapter/10.1007/978-1-62703-035-9_2. Accessed June 20, 2014.
50. 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 and tail. Asian J Androl 2012;14:14-23.
51. Chemes EH, Rawe YV. Sperm pathology: a step beyond descriptive morphology. Origin, characterization and fertility potential of abnormal sperm phenotypes in infertile men. Hum Reprod Update 2003;9:405-428.
52. Chemes HE, Rawe VY. The making of abnormal spermatozoa: cellular and molecular mechanisms underlying pathological spermiogenesis. Cell Tissue Res 2010; 341:349-357.
53. Chemes HE, Brugo 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;48:664-669.
54. 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;13:2521-2526.
55. Chen H-L, Tang C-JC, Chen C-Y, Tang TK. Overexpression of an Aurora-C kinase-deficient mutant disrupts the Aurora-B/INCENP complex and induces polyploidy. J Biomed Sci 2005;12:297-310.
56. Chianese C, Fino MG, Riera Escamilla A, López Rodrigo O, Vinci S, Guarducci E, Daguin F, Muratori M, Tamburrino L, Lo Giacco D et al. Comprehensive investigation in patients affected by sperm macrocephaly and globozoospermia. Andrology 2015;3:203-212.
57. Christensen GL, Ivanov IP, Atkins JF, Campbell B, Carrell DT. Identification of polymorphisms in the Hrb, GOPC, and Csnk2a2 genes in two men with globozoospermia. J Androl 2006;27:11-15.
58. Collodel G, Moretti E. Sperm morphology and aneuploidies: defects of supposed genetic origin. Andrologia 2006;38:208-215.
59. Coutton C, Zouari R, Abada F, Ben Khelifa M, Merdassi G, Triki C, Escalier D, Hesters L, Mitchell V, Levy R et al. MLPA and sequence analysis of DPY19L2 reveals point mutations causing globozoospermia. Hum Reprod 2012; 27:2549-2558.
60. Coutton C, Abada F, Karaouzene T, Sanlaville D, Satre V, Lunardi J, Jouk P-S, Arnoult C, Thierry-Mieg N, Ray PF. Fine characterisation of a recombination hotspot at the DPY19L2 locus and resolution of the paradoxical excess of duplications over deletions in the general population. PLoS Genet 2013;9:e1003363.
61. Dale B, Iaccarino M, Fortunato A, Gragnaniello G, Kyozuka K, Tosti E. Amorphological and functional study of fusibility in round-headed spermatozoa in the human. Fertil Steril 1994;61:336-340.
62. Dam AHDM, Feenstra I, Westphal JR, Ramos L, van Golde RJT, Kremer JAM. Globozoospermia revisited. Hum Reprod Update 2007a;13:63-75.
63. Dam AHDM, Koscinski I, Kremer JAM, Moutou C, Jaeger A-S, Oudakker AR, Tournaye H, Charlet N, Lagier-Tourenne C, van Bokhoven H et al. Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. Am J Hum Genet 2007b;81:813-820.
64. 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.
65. Daniels MLA, Leigh MW, Davis SD, Armstrong MC, Carson JL, Hazucha M, Dell SD, Eriksson M, Collins FS, Knowles MR et al. Founder mutation in RSPH4A identified in patients of Hispanic descent with primary ciliary dyskinesia. Hum Mutat 2013; 34:1352-1356.
66. David G, Feneux D, Serres C, Escalier D, Jouannet P. A new entity of sperm pathology:peri-axonemal flagellar dyskinesia. Bull Académie Natl Médecine 1993;177:263-271; discussion 272-275.
67. Dávila Garza SA, Patrizio P. Reproductive outcomes in patients with male infertility because of Klinefelter's syndrome, Kartagener's syndrome, round-head sperm, dysplasia fibrous sheath, and "stump" tail sperm: an updated literature review. Curr Opin Obstet Gynecol 2013;25:229-246.
68. De Boer P, de Vries M, Ramos L. A mutation study of sperm head shape and motility in the mouse: lessons for the clinic. Andrology 2015;3:174-202.
69. Devillard F, Metzler-Guillemain C, Pelletier R, De Robertis C, Bergues U, Hennebicq S, Guichaoua M, Sèle B, Rousseaux S. Polyploidy in large-headed sperm: FISH study of three cases. Hum Reprod 2002;17:1292-1298.
70. Dieterich K, Soto Rifo R, Faure AK, Hennebicq S, Ben Amar B, Zahi M, Perrin J, Martinez D, Sèle B, Jouk P-S et al. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet 2007; 39:661-665.
71. Dieterich K, Zouari R, Harbuz R, Vialard F, Martinez D, Bellayou H, Prisant N, Zoghmar A, Guichaoua MR, Koscinski I et al. The Aurora Kinase C c.144delC mutation causes meiosis I arrest in men and is frequent in the North African population. Hum Mol Genet 2009;18:1301-1309.
72. Dirami T, Rode B, Jollivet M, Da Silva N, Escalier D, Gaitch N, Norez C, Tuffery P, Wolf J-P, Becq F et al. Missense mutations in SLC26A8, encoding a sperm-specific activator of CFTR, are associated with human asthenozoospermia. Am J Hum Genet 2013;92:760-766.
73. Dirican EK, Isik A, Vicdan K, Sozen E, Suludere Z. Clinical pregnancies and livebirths achieved by intracytoplasmic injection of round headed acrosomeless spermatozoa with and without oocyte activation in familial globozoospermia: case report. Asian J Androl 2008;10:332-336.
74. Duquesnoy P, Escudier E, Vincensini L, Freshour J, Bridoux A-M, Coste A, Deschildre A, de Blic J, Legendre M, Montantin G et al. Loss-of-function mutations in the human ortholog of Chlamydomonas reinhardtii ODA7 disrupt dynein arm assembly and cause primary ciliary dyskinesia. Am J Hum Genet 2009;85:890-896.
75. Duriez B, Duquesnoy P, Escudier E, Bridoux A-M, Escalier D, Rayet I, Marcos E, Vojtek A-M, Bercher J-F, Amselem S. 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;104:3336-3341.
76. Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 2003;61:103-115.
77. Elinati E, Kuentz P, Redin C, Jaber S, Vanden Meerschaut F, Makarian J, Koscinski I, Nasr-Esfahani MH, Demirol A, Gurgan T et al. Globozoospermia is mainly due to DPY19L2 deletion via non-allelic homologous recombination involving two recombination hotspots. Hum Mol Genet 2012;21:3695-3702.
78. 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 2011;40:329-333.
79. Eloualid A, Rouba H, Rhaissi H, Barakat A, Louanjli N, Bashamboo A, McElreavey K. Prevalence of the Aurora kinase C c.144delC mutation in infertile Moroccan men. Fertil Steril 2014;101:1086-1090.
80. Escalier D. Human spermatozoa with large heads and multiple flagella: a quantitative ultrastructural study of 6 cases. Biol Cell 1983;48:65-74.
81. Escalier D, David G. Pathology of the cytoskeleton of the human sperm flagellum:axonemal and peri-axonemal anomalies. Biol Cell 1984;50:37-52.
82. Escalier D, Serres C. Aberrant distribution of the peri-axonemal structures in the human spermatozoon: possible role of the axoneme in the spatial organization of the flagellar components. Biol Cell 1985;53:239-250.
83. Escalier D, Bermùdez D, Gallo JM, Viellefond A, Schrével J. Cytoplasmic events in human meiotic arrest as revealed by immunolabelling of spermatocyte proacrosin. Differentiation 1992;51:233-243.
84. Escoffier J, Yassine S, Lee HC, Martinez G, Delaroche J, Coutton C, Karaouzène T, Zouari R, Metzler-Guillemain C, Pernet-Gallay K et al. Subcellular localization of phospholipase Cz in human sperm and its absence in DPY19L2-deficient sperm are consistent with its role in oocyte activation. Mol Hum Reprod 2015;21:157-168.
85. Failly M, Bartoloni L, Letourneau A, Munoz A, Falconnet E, Rossier C, de Santi MM, Santamaria F, Sacco O, De Lozier-Blanchet CD et al. Mutations in DNAH5 account for only 15% of a non-preselected cohort of patients with primary ciliary dyskinesia. J Med Genet 2009;46:281-286.
86. Fauque P, Albert M, Serres C, Viallon V, Davy C, Epelboin S, Chalas C, Jouannet P, Patrat C. From ultrastructural flagellar sperm defects to the health of babies conceived by ICSI. Reprod Biomed Online 2009;19:326-336.
87. Fernández-Miranda G, Trakala M, Martin J, Escobar B, González A, Ghyselinck NB, Ortega S, Cañamero M, Pérez de Castro I, Malumbres M. Genetic disruption of aurora B uncovers an essential role for aurora C during early mammalian development. Development 2011;138:2661-2672.
88. Fliegauf M, Olbrich H, Horvath J, Wildhaber JH, Zariwala MA, Kennedy M, Knowles MR, Omran H. Mislocalization of DNAH5 and DNAH9 in respiratory cells from patients with primary ciliary dyskinesia. Am J Respir Crit Care Med 2005; 171:1343-1349.
89. 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.
90. Fossella J, Samant SA, Silver LM, King SM, Vaughan KT, Olds-Clarke P, Johnson KA, Mikami A, Vallee RB, Pilder SH. An axonemal dynein at the Hybrid Sterility 6 locus: implications for t haplotype-specific male sterility and the evolution of species barriers. Mamm Genome 2000;11:8-15.
91. Frohnert C, Schweizer S, Hoyer-Fender S. SPAG4L/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol Hum Reprod 2011;17:207-218.
92. Fujihara Y, Satouh Y, Inoue N, Isotani A, Ikawa M, Okabe M. SPACA1-deficient male mice are infertile with abnormally shaped sperm heads reminiscent of globozoospermia. Development 2012;139:3583-3589.
93. Funaki T, Kon S, Tanabe K, Natsume W, Sato S, Shimizu T, Yoshida N, Wong WF, Ogura A, Ogawa T et al. The Arf GAP SMAP2 is necessary for organized vesicle budding from the trans-Golgi network and subsequent acrosome formation in spermiogenesis. Mol Biol Cell 2013;24:2633-2644.
94. German J, Rasch EM, Huang CY, MacLeod J, Imperato-McGinley J. Humaninfertility due to production of multiple-tailed spermatozoa with excessive amounts of DNA. Am Soc Hum Genet 1981;33:64A.
95. Ghedir H, Mehri A, Mehdi M, Brahem S, Saad A, Ibala-Romdhane S. Meiotic segregation and sperm DNA fragmentation in Tunisian men with dysplasia of the fibrous sheath (DFS) associated with head abnormalities. J Assist Reprod Genet 2014;31:1167-1174.
96. Glover DM, Leibowitz MH, McLean DA, Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 1995; 81:95-105.
97. Göb E, Schmitt J, Benavente R, Alsheimer M. Mammalian spermhead formation involves different polarization of two novel LINC complexes. PloS One 2010;5:e12072.
98. Goldenson B, Crispino JD. The aurora kinases in cell cycle and leukemia. Oncogene 2014;34:537-545.
99. Guichard C, Harricane MC, Lafitte JJ, Godard P, Zaegel M, Tack V, Lalau G, Bouvagnet P. Axonemal dynein intermediate-chain gene (DNAI1) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener syndrome). Am J Hum Genet 2001;68:1030-1035.
100. Guthauser B, Vialard F, Dakouane M, Izard V, Albert M, Selva J. Chromosomal analysis of spermatozoa with normal-sized heads in two infertile patients with macrocephalic sperm head syndrome. Fertil Steril 2006;85:750.e5-750.e7.
101. Hao Z, Wolkowicz MJ, Shetty J, Klotz K, Bolling L, Sen B, Westbrook VA, Coonrod S, Flickinger CJ, Herr JC. SAMP32, a testis-specific, isoantigenic sperm acrosomal membrane-associated protein. Biol Reprod 2002;66:735-744.
102. Haraguchi S, Tsuda M, Kitajima S, Sasaoka Y, Nomura-Kitabayashid A, Kurokawa K, Saga Y. nanos1: a mouse nanos gene expressed in the central nervous system is dispensable for normal development. Mech Dev 2003;120:721-731.
103. Harbuz R, Zouari R, Pierre V, Ben Khelifa M, Kharouf M, Coutton C, Merdassi G, Abada F, Escoffier J, Nikas Y et al. A recurrent deletion of DPY19L2 causes infertility in man by blocking sperm head elongation and acrosome formation. Am J Hum Genet 2011;88:351-361.
104. Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon S-Y, Fissore RA, Hamer R, Deane CM, Ruas M et al. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod 2009;24:2417-2428.
105. Hjeij R, Lindstrand A, Francis R, Zariwala MA, Liu X, Li Y, Damerla R, Dougherty GW, Abouhamed M, Olbrich H et al. ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry. Am J Hum Genet 2013; 93:357-367.
106. Hjeij R, Onoufriadis A, Watson CM, Slagle CE, Klena NT, Dougherty GW, Kurkowiak M, Loges NT, Diggle CP, Morante NFC et al. CCDC151 mutations cause primary ciliary dyskinesia by disruption of the outer dynein arm docking complex formation. Am J Hum Genet 2014;95:257-274.
107. Holstein AF, Schirren C, Schirren CG. Human spermatids and spermatozoa lacking acrosomes. J Reprod Fertil 1973;35:489-491.
108. Honigberg L, Kenyon C. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 2000;127:4655-4668.
109. Horani A, Druley TE, Zariwala MA, Patel AC, Levinson BT, Van Arendonk LG, Thornton KC, Giacalone JC, Albee AJ, Wilson KS et al. Whole-exome capture and sequencing identifies HEATR2 mutation as a cause of primary ciliary dyskinesia. Am J Hum Genet 2012;91:685-693.
110. Horani A, Ferkol TW, Shoseyov D, Wasserman MG, Oren YS, Kerem B, Amirav I, Cohen-Cymberknoh M, Dutcher SK, Brody SL et al. LRRC6 mutation causes primary ciliary dyskinesia with dynein arm defects. PloS One 2013a;8:e59436.
111. Horani A, Brody SL, Ferkol TW, Shoseyov D, Wasserman MG, Ta-shma A, Wilson KS, Bayly PV, Amirav I, Cohen-Cymberknoh M et al. CCDC65 mutation causes primary ciliary dyskinesia with normal ultrastructure and hyperkinetic cilia. PloS One 2013b; 8:e72299.
112. Horani A, Brody SL, Ferkol TW. Picking up speed: advances in the genetics of primary ciliary dyskinesia. Pediatr Res 2014;75:158-164.
113. Hornef N, Olbrich H, Horvath J, Zariwala MA, Fliegauf M, Loges NT, Wildhaber J, Noone PG, Kennedy M, Antonarakis SE et al. DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am J Respir Crit Care Med 2006;174:120-126.
114. Ibañez-Tallon I, Gorokhova S, Heintz N. Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 2002; 11:715-721.
115. Ibañez-Tallon I, Heintz N, Omran H. To beat or not to beat: roles of cilia in development and disease. Hum Mol Genet 2003;12(Spec No 1):R27-R35.
116. Ikegami K, Sato S, Nakamura K, Ostrowski LE, Setou M. Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry. Proc Natl Acad Sci USA 2010;107:10490-10495.
117. In't Veld PA, Broekmans FJ, de France HF, Pearson PL, Pieters MH, van Kooij RJ. Intracytoplasmic sperm injection (ICSI) and chromosomally abnormal spermatozoa. Hum Reprod 1997;12:752-754.
118. Inaba K. Molecular architecture of the sperm flagella: molecules for motility and signaling. Zoolog Sci 2003;20:1043-1056.
119. Inaba K. Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod 2011;17:524-538.
120. Ito C, Suzuki-Toyota F, Maekawa M, Toyama Y, Yao R, Noda T, Toshimori K. Failure to assemble the peri-nuclear structures in GOPC deficient spermatids as found in round-headed spermatozoa. Arch Histol Cytol 2004;67:349-360.
121. Jeganathan D, Chodhari R, Meeks M, Faeroe O, Smyth D, Nielsen K, Amirav I, Luder AS, Bisgaard H, Gardiner RM et al. Loci for primary ciliary dyskinesia map to chromosome 16p12.1-12.2 and 15q13.1-15.1 in Faroe Islands and Israeli Druze genetic isolates. J Med Genet 2004;41:233-240.
122. Jerber J, Baas D, Soulavie F, Chhin B, Cortier E, Vesque C, Thomas J, Durand B. The coiled-coil domain containing protein CCDC151 is required for the function of IFT-dependent motile cilia in animals. Hum Mol Genet 2014;23:563-577.
123. Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C, European Association of Urology Working Group on Male Infertility. European Association of Urology guidelines on Male Infertility: the 2012 update. Eur Urol 2012;62:324-332.
124. Kahraman S, Akarsu C, Cengiz G, Dirican K, Sözen E, Can B, Güven C, Vanderzwalmen P. Fertility of ejaculated and testicular megalohead spermatozoa with intracytoplasmic sperm injection. Hum Reprod 1999;14:726-730.
125. Kahraman S, Sertyel S, Findikli N, Kumtepe Y, Oncu N, Melil S, Unal S, Yelke H, Vanderzwalmen P. Effect of PGD on implantation and ongoing pregnancy rates in cases with predominantly macrocephalic spermatozoa. Reprod Biomed Online 2004;9:79-85.
126. Kang-Decker N, Mantchev GT, Juneja SC, McNiven MA, van Deursen JM. Lack of acrosome formation in Hrb-deficient mice. Science 2001;294:1531-1533.
127. Karaca N, Yilmaz R, Kanten GE, Kervancioglu E, Solakoglu S, Kervancioglu ME. First successful pregnancy in a globozoospermic patient having homozygous mutation in SPATA16. Fertil Steril 2014;102:103-107.
128. Karaouzène T, El Atifi M, Issartel J-P, Grepillat M, Coutton C, Martinez D, Arnoult C, Ray P. Comparative testicular transcriptome of wild type and globozoospermic Dpy19l2 knock out mice. Basic Clin Androl 2013;23. Available at: http://hal. univ-grenoble-alpes.fr/inserm-00880088/. Accessed May 7, 2014.
129. Kashir J, Heindryckx B, Jones C, Sutter PD, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update 2010;16:690-703.
130. Kaufmann KB, Büning H, Galy A, Schambach A, Grez M. Gene therapy on the move. EMBO Mol Med 2013;5:1642-1661.
131. Khan J, Ezan F, Crémet J-Y, Fautrel A, Gilot D, Lambert M, Benaud C, Troadec M-B, Prigent C. Overexpression of active Aurora-C kinase results in cell transformation and tumour formation. PLoS One 2011;6:e26512.
132. Khattri A, Reddy VP, Pandey RK, Sudhakar DVS, Gupta NJ, Chakravarty BN, Deenadayal M, Singh L, Thangaraj K. Novel mutations in calcium/calmodulin-dependent protein kinase IV (CAMK4) gene in infertile men. Int J Androl 2012;35:810-818.
133. Kierszenbaum AL, Tres LL, Rivkin E, Kang-Decker N, van Deursen JMA. The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/bcontaining proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids. Biol Reprod 2004;70:1400-1410.
134. Kilani Z, Ismail R, Ghunaim S, Mohamed H, Hughes D, Brewis I, Barratt CLR. Evaluation and treatment of familial globozoospermia in five brothers. Fertil Steril 2004; 82:1436-1439.
135. Kimmins S, Crosio C, Kotaja N, Hirayama J, Monaco L, Höög C, van Duin M, Gossen JA, Sassone-Corsi P. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 2007;21:726-739.
136. King SM. Asolid-state control systemfor dynein-based ciliary/flagellar motility. J Cell Biol 2013;201:173-175.
137. Knowles MR, Leigh MW, Carson JL, Davis SD, Dell SD, Ferkol TW, Olivier KN, Sagel SD, Rosenfeld M, Burns KA et al. Mutations of DNAH11 in patients with primary ciliary dyskinesia with normal ciliary ultrastructure. Thorax 2012;67:433-441.
138. Knowles MR, Daniels LA, Davis SD, Zariwala MA, Leigh MW. Primary ciliary dyskinesia. Recent advances in diagnostics, genetics, and characterization of clinical disease. AmJ Respir Crit Care Med 2013a;188:913-922.
139. Knowles MR, Leigh MW, Ostrowski LE, Huang L, Carson JL, Hazucha MJ, Yin W, Berg JS, Davis SD, Dell SD et al. Exome sequencing identifies mutations in CCDC114 as a cause of primary ciliary dyskinesia. Am J Hum Genet 2013b; 92:99-106.
140. Knowles MR, Ostrowski LE, Loges NT, Hurd T, Leigh MW, Huang L, Wolf WE, Carson JL, Hazucha MJ, Yin W et al. Mutations in SPAG1 cause primary ciliary dyskinesia associated with defective outer and inner dynein arms. Am J Hum Genet 2013c;93:711-720.
141. Knowles MR, Ostrowski LE, Leigh MW, Sears PR, Davis SD, Wolf WE, Hazucha MJ, Carson JL, Olivier KN, Sagel SD et al. Mutations in RSPH1 cause primary ciliary dyskinesia with a unique clinical and ciliary phenotype. Am J Respir Crit Care Med 2014;189:707-717.
142. Kosaki K, Ikeda K, Miyakoshi K, Ueno M, Kosaki R, Takahashi D, Tanaka M, Torikata C, Yoshimura Y, Takahashi T. Absent inner dynein arms in a fetus with familial hydrocephalus-situs abnormality. Am J Med Genet A 2004;129A:308-311.
143. Koscinski I, Elinati E, Fossard C, Redin C, Muller J, Velez de la Calle J, Schmitt F, Ben Khelifa M, Ray PF, Ray P et al. DPY19L2 deletion as a major cause of globozoospermia. Am J Hum Genet 2011;88:344-350.
144. Kott E, Duquesnoy P, Copin B, Legendre M, Dastot-Le Moal F, Montantin G, Jeanson L, Tamalet A, Papon J-F, Siffroi J-P et al. Loss-of-function mutations in LRRC6, a gene essential for proper axonemal assembly of inner and outer dynein arms, cause primary ciliary dyskinesia. Am J Hum Genet 2012;91:958-964.
145. Kott E, Legendre M, Copin B, Papon J-F, Dastot-Le Moal F, Montantin G, Duquesnoy P, Piterboth W, Amram D, Bassinet L et al. Loss-of-function mutations in RSPH1 cause primary ciliary dyskinesia with central-complex and radial-spoke defects. Am J Hum Genet 2013;93:561-570.
146. Krausz C. Male infertility: pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab 2011;25:271-285.
147. Krausz C, Hoefsloot L, Simoni M, Tüttelmann F, European Academy of Andrology, European Molecular Genetics Quality Network. EAA/EMQN best practice guidelines for molecular diagnosis of Y-chromosomal microdeletions:state-of-the-art 2013. Andrology 2014;2:5-19.
148. Kruger TF, Menkveld R, Stander FS, Lombard CJ, Van der Merwe JP, van Zyl JA, Smith K. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 1986;46:1118-1123.
149. Kuentz P, Vanden Meerschaut F, Elinati E, Nasr-Esfahani MH, Gurgan T, Iqbal N, Carré-Pigeon F, Brugnon F, Gitlin SA, Velez de la Calle J et al. Assisted oocyte activation overcomes fertilization failure in globozoospermic patients regardless of the DPY19L2 status. Hum Reprod 2013;28:1054-1061.
150. Kullander S, Rausing A. On round-headed human spermatozoa. Int J Fertil 1975; 20:33-40.
151. Kuo Y-C, Lin Y-H, Chen H-I, Wang Y-Y, Chiou Y-W, Lin H-H, Pan H-A, Wu C-M, Su S-M, Hsu C-C et al. SEPT12 mutations cause male infertility with defective sperm annulus. Hum Mutat 2012;33:710-719.
152. Kusz-Zamelczyk K, Sajek M, Spik A, Glazar R, Jędrzejczak P, Latos-Bieleńska A, Kotecki M, Pawelczyk L, Jaruzelska J. Mutations of NANOS1, a human homologue of the Drosophila morphogen, are associated with a lack of germ cells in testes or severe oligo-astheno-teratozoospermia. J Med Genet 2013;50:187-193.
153. Kyono K, Nakajo Y, Nishinaka C, Hattori H, Kyoya T, Ishikawa T, Abe H, Araki Y. A birth from the transfer of a single vitrified-warmed blastocyst using intracytoplasmic sperm injection with calcium ionophore oocyte activation in a globozoospermic patient. Fertil Steril 2009;91:931.e7-11.
154. Lee L, Campagna DR, Pinkus JL, Mulhern H, Wyatt TA, Sisson JH, Pavlik JA, Pinkus GS, Fleming MD. Primary ciliary dyskinesia in mice lacking the novel ciliary protein Pcdp1. Mol Cell Biol 2008;28:949-957.
155. Lerer-Goldshtein T, Bel S, Shpungin S, Pery E, Motro B, Goldstein RS, Bar-Sheshet SI, Breitbart H, Nir U. TMF/ARA160: a key regulator of sperm development. Dev Biol 2010;348:12-21.
156. Lessard C, Lothrop H, Schimenti JC, Handel MA. Mutagenesis-generated mouse models of human infertility with abnormal sperm. Hum Reprod 2007;22:159-166.
157. Lewis-Jones I, Aziz N, Seshadri S, Douglas A, Howard P. Sperm chromosomal abnormalities are linked to sperm morphologic deformities. Fertil Steril 2003; 79:212-215.
158. Li X, Sakashita G, Matsuzaki H, Sugimoto K, Kimura K, Hanaoka F, Taniguchi H, Furukawa K, Urano T. Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. J Biol Chem 2004;279:47201-47211.
159. Lin Y-N, Roy A, Yan W, Burns KH, Matzuk MM. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol 2007;27:6794-6805.
160. Lin Y-H, Wang Y-Y, Chen H-I, Kuo Y-C, Chiou Y-W, Lin H-H, Wu C-M, Hsu C-C, Chiang H-S, Kuo P-L. SEPTIN12 genetic variants confer susceptibility to teratozoospermia. PLoS One 2012;7:e34011.
161. Liu G, Shi Q-W, Lu G-X. A newly discovered mutation in PICK1 in a human with globozoospermia. Asian J Androl 2010;12:556-560.
162. Liu P, Carvalho CMB, Hastings PJ, Lupski JR. Mechanisms for recurrent and complex human genomic rearrangements. Curr Opin Genet Dev 2012;22:211-220.
163. Loges NT, Olbrich H, Fenske L, Mussaffi H, Horvath J, Fliegauf M, Kuhl H, Baktai G, Peterffy E, Chodhari R et al. DNAI2 mutations cause primary ciliary dyskinesia with defects in the outer dynein arm. Am J Hum Genet 2008;83:547-558.
164. Loges NT, Olbrich H, Becker-Heck A, Häffner K, Heer A, Reinhard C, Schmidts M, Kispert A, Zariwala MA, Leigh MW et al. Deletions and point mutations of LRRC50 cause primary ciliary dyskinesia due to dynein arm defects. Am J Hum Genet 2009;85:883-889.
165. Lu L, Lin M, Xu M, Zhou Z-M, Sha J-H. Gene functional research using polyethylenimine-mediated in vivo gene transfection into mouse spermatogenic cells. Asian J Androl 2006;8:53-59.
166. Lucas JS, Adam EC, Goggin PM, Jackson CL, Powles-Glover N, Patel SH, Humphreys J, Fray MD, Falconnet E, Blouin J-L et al. Static respiratory cilia associated with mutations in Dnahc11/DNAH11: a mouse model of PCD. Hum Mutat 2012; 33:495-503.
167. Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update 2006;12:363-372.
168. Maiti AK, Mattéi MG, Jorissen M, Volz A, Zeigler A, Bouvagnet P. Identification, tissue specific expression, and chromosomal localisation of several human dynein heavy chain genes. Eur J Hum Genet 2000;8:923-932.
169. Mannowetz N, Kartarius S, Wennemuth G, Montenarh M. Protein kinase CK2 andnewbinding partners during spermatogenesis. Cell Mol Life Sci 2010;67:3905-3913.
170. Mateu E, Rodrigo L, Prados N, Gil-Salom M, Remohi J, Pellicer A, Rubio C. High incidence of chromosomal abnormalities in large-headed and multiple-tailed spermatozoa. J Androl 2006;27:6-10.
171. Matzuk MM, Lamb DJ. Genetic dissection of mammalian fertility pathways. Nat Cell Biol 2002;4(Suppl):s41-s49.
172. Matzuk MM, Lamb DJ. The biology of infertility: research advances and clinical challenges. Nat Med 2008;14:1197-1213.
173. Mazor M, Alkrinawi S, Chalifa-Caspi V, Manor E, Sheffield VC, Aviram M, Parvari R. Primary ciliary dyskinesia caused by homozygous mutation in DNAL1, encoding dynein light chain 1. Am J Hum Genet 2011;88:599-607.
174. Merveille A-C, Davis EE, Becker-Heck A, Legendre M, Amirav I, Bataille G, Belmont J, Beydon N, Billen F, Clément A et al. CCDC39 is required for assembly of inner dynein arms and the dynein regulatory complex and for normal ciliary motility in humans and dogs. Nat Genet 2011;43:72-78.
175. Miki K, Willis WD, Brown PR, Goulding EH, Fulcher KD, Eddy EM. Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 2002; 248:331-342.
176. Mitchell V, Rives N, Albert M, Peers M-C, Selva J, Clavier B, Escudier E, Escalier D. Outcome of ICSI with ejaculated spermatozoa in a series of men with distinct ultrastructural flagellar abnormalities. Hum Reprod 2006;21:2065-2074.
177. Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, O'Callaghan C, Blau H, Al Dabbagh M, Olbrich H et al. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet 2012; 44:381-389, S1-2.
178. 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;26:148-156.
179. Moore A, Escudier E, Roger G, Tamalet A, Pelosse B, Marlin S, Clément A, Geremek M, Delaisi B, Bridoux A-M et al. RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J Med Genet 2006;43:326-333.
180. Moore DJ, Onoufriadis A, Shoemark A, Simpson MA, zur Lage PI, de Castro SC, Bartoloni L, Gallone G, Petridi S, Woollard WJ et al. Mutations in ZMYND10, a gene essential for proper axonemal assembly of inner and outer dynein arms in humans and flies, cause primary ciliary dyskinesia. Am J Hum Genet 2013; 93:346-356.
181. Moretti E, Geminiani M, Terzuoli G, Renieri T, Pascarelli N, Collodel G. Two cases of sperm immotility: a mosaic of flagellar alterations related to dysplasia of the fibrous sheath and abnormalities of head-neck attachment. Fertil Steril 2011;95:1787.e19-23.
182. Munro NC, Currie DC, Lindsay KS, Ryder TA, Rutman A, Dewar A, Greenstone MA, Hendry WF, Cole PJ. Fertility in men with primary ciliary dyskinesia presenting with respiratory infection. Thorax 1994;49:684-687.
183. Musacchio A, Hardwick KG. The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 2002;3:731-741.
184. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 2010;327:876-879.
185. Nakamura N, Dai Q, Williams J, Goulding EH, Willis WD, Brown PR, Eddy EM. Disruption of a spermatogenic cell-specific mouse enolase 4 (eno4) gene causes sperm structural defects and male infertility. Biol Reprod 2013;88:90.
186. Neesen J, Kirschner R, Ochs M, Schmiedl A, Habermann B, Mueller C, Holstein AF, Nuesslein T, Adham I, Engel W. Disruption of an inner arm dynein heavy chain gene results in asthenozoospermia and reduced ciliary beat frequency. Hum Mol Genet 2001;10:1117-1128.
187. 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 shortmidpiece. Hum Reprod 1990;5:981-986.
188. Nieschlag E, Behre HM, Nieschlag S. Andrology: Male Reproductive Health and Dysfunction. Springer Science & Business Media, 2010.
189. Nistal M, Paniagua R, Herruzo A. Multi-tailed spermatozoa in a case with asthenospermia and teratospermia. Virchows Arch B Cell Pathol 1977;26:111-118.
190. Noveski P, Madjunkova S, Maleva I, Sotiroska V, Petanovski Z, Plaseska-Karanfilska D. A homozygous deletion of the DPY19l2 gene is a cause of globozoospermia in men from the Republic of Macedonia. Balk J Med Genet 2013;16:73-76.
191. O'Callaghan C, Chetcuti P, Moya E. High prevalence of primary ciliary dyskinesia in a British Asian population. Arch Dis Child 2010;95:51-52.
192. Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 1997;41:111-122.
193. Olbrich H, Häffner K, Kispert A, Völkel A, Volz A, Sasmaz G, Reinhardt R, Hennig S, Lehrach H, Konietzko N et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 2002;30:143-144.
194. Olbrich H, Schmidts M, Werner C, Onoufriadis A, Loges NT, Raidt J, Banki NF, Shoemark A, Burgoyne T, Al Turki S et al. Recessive HYDIN mutations cause primary ciliary dyskinesia without randomization of left-right body asymmetry. Am J Hum Genet 2012;91:672-684.
195. Olmedo SB, Nodar F, Chillik C, Chemes HE. Successful intracytoplasmic sperm injection with spermatozoa from a patient with dysplasia of the fibrous sheath and chronic respiratory disease. Hum Reprod 1997;12:1497-1499.
196. 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;2:125-130.
197. Ombelet W, Menkveld R, Kruger TF, Steeno O. Sperm morphology assessment:historical review in relation to fertility. Hum Reprod Update 1995;1:543-557.
198. Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, Hagiwara H, Zhang Q, Leblond G, O'Toole E, Hara C et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 2008;456:611-616.
199. Onoufriadis A, Paff T, Antony D, Shoemark A, Micha D, Kuyt B, Schmidts M, Petridi S, Dankert-Roelse JE, Haarman EG et al. Splice-site mutations in the axonemal outer dynein arm docking complex gene CCDC114 cause primary ciliary dyskinesia. Am J Hum Genet 2013;92:88-98.
200. Onoufriadis A, Shoemark A, Munye MM, James CT, Schmidts M, Patel M, Rosser EM, Bacchelli C, Beales PL, Scambler PJ et al. Combined exome and whole-genome sequencing identifies mutations in ARMC4 as a cause of primary ciliary dyskinesia with defects in the outer dynein arm. J Med Genet 2014a;51:61-67.
201. Onoufriadis A, Shoemark A, Schmidts M, Patel M, Jimenez G, Liu H, Thomas B, Dixon M, Hirst RA, Rutman A et al. Targeted NGS gene panel identifies mutations in RSPH1 causing primary ciliary dyskinesia and a common mechanism for ciliary central pair agenesis due to radial spoke defects. Hum Mol Genet 2014b; 23:3362-3374.
202. Ostrowski LE, Dutcher SK, Lo CW. Cilia and models for studying structure and function. Proc Am Thorac Soc 2011;8:423-429.
203. Ounis L, Zoghmar A, Coutton C, Rouabah L, Hachemi M, Martinez D, Martinez G, Bellil I, Khelifi D, Arnoult C et al. 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.
204. Paiardi C, Pasini ME, Gioria M, Berruti G. Failure of acrosome formation and globozoospermia in the wobbler mouse, a Vps54 spontaneous recessive mutant. Spermatogenesis 2011;1:52-62.
205. Palermo GD, Neri QV, Takeuchi T, Rosenwaks Z. ICSI: wherewehave been and where we are going. Semin Reprod Med 2009;27:191-201.
206. Panizzi JR, Becker-Heck A, Castleman VH, Al-Mutairi DA, Liu Y, Loges NT, Pathak N, Austin-Tse C, Sheridan E, Schmidts M et al. CCDC103 mutations cause primary ciliary dyskinesia by disrupting assembly of ciliary dynein arms. Nat Genet 2012; 44:714-719.
207. Parvanov ED, Petkov PM, Paigen K. Prdm9 controls activation of mammalian recombination hotspots. Science 2010;327:835.
208. Pennarun G, Escudier E, Chapelin C, Bridoux AM, Cacheux V, Roger G, Clément A, Goossens M, Amselem S, Duriez B. Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 1999;65:1508-1519.
209. Perrin A, Morel F, Moy L, Colleu D, Amice V, De Braekeleer M. Study of aneuploidy in large-headed, multiple-tailed spermatozoa: case report and review of the literature. Fertil Steril 2008;90:1201.e13-1201.e17.
210. Perrin A, Coat C, Nguyen MH, Talagas M, Morel F, Amice J, De Braekeleer M. Molecular cytogenetic and genetic aspects of globozoospermia: a review. Andrologia 2013;45:1-9.
211. Pierre V, Martinez G, Coutton C, Delaroche J, Yassine S, Novella C, Pernet-Gallay K, Hennebicq S, Ray PF, Arnoult C. Absence of Dpy19l2, a new inner nuclear membrane protein, causes globozoospermia in mice by preventing the anchoring of the acrosome to the nucleus. Development 2012;139:2955-2965.
212. Pieters MH, Speed RM, de Boer P, Vreeburg JT, Dohle G, In't Veld PA. Evidence of disturbed meiosis in a man referred for intracytoplasmic sperm injection. Lancet 1998;351:957.
213. Pigino G, Bui KH, Maheshwari A, Lupetti P, Diener D, Ishikawa T. Cryoelectron tomography of radial spokes in cilia and flagella. J Cell Biol 2011;195:673-687.
214. Pilder SH, Olds-Clarke P, Orth JM, Jester WF, Dugan L. Hst7: a male sterility mutation perturbing sperm motility, flagellar assembly, and mitochondrial sheath differentiation. J Androl 1997;18:663-671.
215. Pirrello O, Machev N, Schimdt F, Terriou P, Ménézo Y, Viville S. Search for mutations involved in human globozoospermia. Hum Reprod 2005;20:1314-1318.
216. Poongothai J, Gopenath TS, Manonayaki S. Genetics of human male infertility. Singapore Med J 2009;50:336-347.
217. Popli K, Stewart J. Infertility and its management in men with cystic fibrosis:review of literature and clinical practices in the UK. Hum Fertil (Camb) 2007; 10:217-221.
218. Price DM, Kanyo R, Steinberg N, Chik CL, Ho AK. Nocturnal activation of aurora C in rat pineal gland: its role in the norepinephrine-induced phosphorylation of histone H3 and gene expression. Endocrinology 2009;150:2334-2341.
219. Rawe VY, Galaverna GD, Acosta AA, Olmedo SB, Chemes HE. Incidence of tail structure distortions associated with dysplasia of the fibrous sheath in human spermatozoa. Hum Reprod 2001;16:879-886.
220. Rawe VY, Terada Y, Nakamura S, Chillik CF, Olmedo SB, Chemes HE. A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Hum Reprod 2002;17:2344-2349.
221. Rives N, Mousset-Simeon N, Mazurier S, Mace B. Primary flagellar abnormality is associated with an increased rate of spermatozoa aneuploidy. J Androl 2005;26:61-69.
222. Rybouchkin AV, Van der Straeten F, Quatacker J, DeSutter P, Dhont M. Fertilization and pregnancy after assisted oocyte activation and intracytoplasmic sperm injection in a case of round-headed sperm associated with deficient oocyte activation capacity. Fertil Steril 1997;68:1144-1147.
223. Salzberg Y, Eldar T, Karminsky O-D, Itach SB-S, Pietrokovski S, Don J. Meig1 deficiency causes a severe defect in mouse spermatogenesis. Dev Biol 2010; 338:158-167.
224. Sapiro R, Tarantino LM, Velazquez F, Kiriakidou M, Hecht NB, Bucan M, Strauss JF. Sperm antigen 6 is the murine homologue of the Chlamydomonas reinhardtii central apparatus protein encoded by the PF16 locus. Biol Reprod 2000;62:511-518.
225. Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, Strauss III JF. Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 2002;22:6298-6305.
226. Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M, Suzuki F, Nigg EA et al. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 2004;59:249-263.
227. Sathananthan AH. Functional competence of abnormal spermatozoa. Baillières Clin Obstet Gynaecol 1994;8:141-156.
228. Sathananthan AH, Kola I, Osborne J, Trounson A, Ng SC, Bongso A, Ratnam SS. Centrioles in the beginning of human development. Proc Natl Acad Sci USA 1991; 88:4806-4810.
229. Satir P, Christensen ST. Structure and function of mammalian cilia. Histochem Cell Biol 2008;129:687-693.
230. Schatten H, Sun Q-Y. The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 2009;50:620-636.
231. Schindler K, Davydenko O, Fram B, Lampson MA, Schultz RM. Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development. Proc Natl Acad Sci USA 2012;109:E2215-E2222.
232. Schwabe GC, Hoffmann K, Loges NT, Birker D, Rossier C, de Santi MM, Olbrich H, Fliegauf M, Failly M, Liebers U et al. Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Hum Mutat 2008;29:289-298.
233. Sen CGS, Holstein AF, Schirren C. über die Morphogenese rundköpfiger Spermatozoen des Menschen. Andrologia 1971;3:117-125.
234. Sermondade N, Hafhouf E, Dupont C, Bechoua S, Palacios C, Eustache F, Poncelet C, Benzacken B, Lévy R, Sifer C. Successful childbirth after intracytoplasmic morphologically selected sperm injection without assisted oocyte activation in a patient with globozoospermia. Hum Reprod 2011;26:2944-2949.
235. Sha Y-W, Ding L, Li P. Management of primary ciliary dyskinesia/Kartagener's syndrome in infertile male patients and current progress in defining the underlying genetic mechanism. Asian J Androl 2014;16:101-106.
236. Sharif B, Na J, Lykke-Hartmann K, McLaughlin SH, Laue E, Glover DM, Zernicka-Goetz M. The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J Cell Sci 2010;123:4292-4300.
237. Singh G. Ultrastructural features of round-headed human spermatozoa. Int J Fertil 1992; 37:99-102.
238. Sironen A, Thomsen B, Andersson M, Ahola V, Vilkki J. An intronic insertion in KPL2 results in aberrant splicing and causes the immotile short-tail sperm defect in the pig. Proc Natl Acad Sci USA 2006;103:5006-5011.
239. Sironen A, Hansen J, Thomsen B, Andersson M, Vilkki J, Toppari J, Kotaja N. Expression of SPEF2 duringmouse spermatogenesis and identification of IFT20 as an interacting protein. Biol Reprod 2010;82:580-590.
240. Sironen A, Kotaja N, Mulhern H, Wyatt TA, Sisson JH, Pavlik JA, Miiluniemi M, Fleming MD, Lee L. Loss of SPEF2 function in mice results in spermatogenesis defects and primary ciliary dyskinesia. Biol Reprod 2011;85:690-701.
241. Smith EN, Bloss CS, Badner JA, Barrett T, Belmonte PL, Berrettini W, Byerley W, Coryell W, Craig D, Edenberg HJ et al. Genome-wide association study of bipolar disorder in European American and African American individuals. Mol Psychiatry 2009;14:755-763.
242. Stalf T, Sánchez R, Köhn FM, Schalles U, Kleinstein J, Hinz V, Tielsch J, Khanaga O, Turley H, Gips H. Pregnancy and birth after intracytoplasmic sperm injection with spermatozoa from a patient with tail stump syndrome. Hum Reprod 1995; 10:2112-2114.
243. Stankiewicz P, Lupski JR. Structural variation in the human genome and its role in disease. Annu Rev Med 2010;61:437-455.
244. Sun F, Ko E, Martin RH. Is there a relationship between sperm chromosome abnormalities and sperm morphology? Reprod Biol Endocrinol 2006;4:1.
245. Sunkel CE, Glover DM. Polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J Cell Sci 1988;89:25-38.
246. Tang C-JC, Lin C-Y, Tang TK. Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol 2006;290:398-410.
247. Tarkar A, Loges NT, Slagle CE, Francis R, Dougherty GW, Tamayo JV, Shook B, Cantino M, Schwartz D, Jahnke C et al. DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nat Genet 2013;45:995-1003.
248. Taylor SL, Yoon SY, Morshedi MS, Lacey DR, Jellerette T, Fissore RA, Oehninger S. Complete globozoospermia associated with PLCz deficiency treated with calcium ionophore and ICSI results in pregnancy. Reprod Biomed Online 2010;20:559-564.
249. Tejera A, Mollá M, Muriel L, Remohi J, Pellicer A, De Pablo JL. Successful pregnancy and childbirth after intracytoplasmic sperm injection with calcium ionophore oocyte activation in a globozoospermic patient. Fertil Steril 2008;90:1202.e1-1202.e5.
250. Terada Y, Nakamura S, Morita J, Tachibana M, Morito Y, Ito K, Murakami T, Yaegashi N, Okamura K. Use of mammalian eggs for assessment of human sperm function:molecular and cellular analyses of fertilization by intracytoplasmic sperm injection. Am J Reprod Immunol 2004;51:290-293.
251. Teves ME, Jha KN, Song J, Nagarkatti-Gude DR, Herr JC, Foster JA, Strauss JF, Zhang Z. Germ cell-specific disruption of the Meig1 gene causes impaired spermiogenesis in mice. Andrology 2013;1:37-46.
252. Thonneau P, Marchand S, Tallec A, Ferial ML, Ducot B, Lansac J, Lopes P, Tabaste JM, Spira A. Incidence and main causes of infertility in a resident population (1,850,000) of three French regions (1988-1989). Hum Reprod 1991;6:811-816.
253. Tseng TC, Chen SH, Hsu YP, Tang TK. Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol 1998; 17:823-833.
254. Tsou J-H, Chang K-C, Chang-Liao P-Y, Yang S-T, Lee C-T, Chen Y-P, Lee Y-C, Lin B-W, Lee J-C, Shen M-R et al. Aberrantly expressed AURKCenhances the transformation and tumourigenicity of epithelial cells. J Pathol 2011;225:243-254.
255. Turner RM, Musse MP, Mandal A, Klotz K, Jayes FC, Herr JC, Gerton GL, Moss SB, Chemes HE. Molecular genetic analysis of two human sperm fibrous sheath proteins, AKAP4 and AKAP3, in men with dysplasia of the fibrous sheath. J Androl 2001;22:302-315.
256. Turner DJ, Miretti M, Rajan D, Fiegler H, Carter NP, Blayney ML, Beck S, Hurles ME. Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat Genet 2008;40:90-95.
257. Tüttelmann F, Simoni M, Kliesch S, Ledig S, Dworniczak B, Wieacker P, Röpke A. Copy number variants in patients with severe oligozoospermia and Sertoli-cell-only syndrome. PLoS One 2011a;6:e19426.
258. Tüttelmann F, Werny F, Cooper TG, Kliesch S, Simoni M, Nieschlag E. Clinical experience with azoospermia: aetiology and chances for spermatozoa detection upon biopsy. Int J Androl 2011b;34:291-298.
259. Vader G, Maia AF, Lens SM. The chromosomal passenger complex and the spindle assembly checkpoint: kinetochore-microtubule error correction and beyond. Cell Div 2008;3:10.
260. Vagnarelli P, Earnshaw WC. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 2004;113:211-222.
261. Van Blerkom J. Sperm centrosome dysfunction: a possible new class of male factor infertility in the human. Mol Hum Reprod 1996;2:349-354.
262. Van der Horst A, Lens SMA. Cell division: control of the chromosomal passenger complex in time and space. Chromosoma 2014;123:25-42.
263. Van der Waal MS, Hengeveld RCC, van der Horst A, Lens SMA. Cell division control by the Chromosomal Passenger Complex. Exp Cell Res 2012;318:1407-1420.
264. Vernon GG, Neesen J, Woolley DM. Further studies on knockout mice lacking a functional dynein heavy chain (MDHC7). 1. Evidence for a structural deficit in the axoneme. Cell Motil Cytoskeleton 2005;61:65-73.
265. Vicari E, de Palma A, Burrello N, Longo G, Grazioso C, Barone N, Zahi M, D'Agata R, Calogero AE. Absolute polymorphic teratozoospermia in patients with oligoasthenozoospermia is associated with an elevated sperm aneuploidy rate. J Androl 2003;24:598-603.
266. Vincensini L, Blisnick T, Bastin P. 1001 model organisms to study cilia and flagella. Biol Cell 2011;103:109-130.
267. Viville S, Mollard R, Bach ML, Falquet C, Gerlinger P, Warter S. Do morphological anomalies reflect chromosomal aneuploidies?: case report. Hum Reprod 2000; 15:2563-2566.
268. Vogel P, Hansen G, Fontenot G, Read R. Tubulin tyrosine ligase-like 1 deficiency results in chronic rhinosinusitis and abnormal development of spermatid flagella in mice. Vet Pathol 2010;47:703-712.
269. Vogt PH, Falcao CL, Hanstein R, Zimmer J. The AZF proteins. Int J Androl 2008; 31:383-394.
270. Walden CM, Sandhoff R, Chuang C-C, Yildiz Y, Butters TD, Dwek RA, Platt FM, van der Spoel AC. Accumulation of glucosylceramide in murine testis, caused by inhibition of beta-glucosidase 2: implications for spermatogenesis. J Biol Chem 2007;282:32655-32664.
271. Wang H, Wan H, Li X, Liu W, Chen Q, Wang Y, Yang L, Tang H, Zhang X, Duan E et al. Atg7 is required for acrosome biogenesis during spermatogenesis in mice. Cell Res 2014;24:852-869.
272. Wargo MJ, Smith EF. Asymmetry of the central apparatus defines the location of active microtubule sliding in Chlamydomonas flagella. Proc Natl Acad Sci USA 2003; 100:137-142.
273. Watanabe K, Takebayashi H, Bepari AK, Esumi S, Yanagawa Y, Tamamaki N. Dpy19l1, a multi-transmembrane protein, regulates the radial migration of glutamatergic neurons in the developing cerebral cortex. Development 2011;138:4979-4990.
274. Weissenberg R, Aviram A, Golan R, Lewin LM, Levron J, Madgar I, Dor J, Barkai G, Goldman B. Concurrent use of flow cytometry and fluorescence in-situ hybridization techniques for detecting faulty meiosis in a human sperm sample. Mol Hum Reprod 1998;4:61-66.
275. Wickstead B, Gull K. Dyneins across eukaryotes: acomparative genomic analysis. Traffic 2007;8:1708-1721.
276. Wirschell M, Olbrich H, Werner C, Tritschler D, Bower R, Sale WS, Loges NT, Pennekamp P, Lindberg S, Stenram U et al. The nexin-dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nat Genet 2013;45:262-268.
277. World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction, 1st edn. Singapore: Press Concern, 1980.
278. World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. Cambridge: Cambridge University Press, 2010, 272 p.
279. Xiao N, Kam C, Shen C, Jin W, Wang J, Lee KM, Jiang L, Xia J. PICK1 deficiency causes male infertility in mice by disrupting acrosome formation. J Clin Invest 2009; 119:802-812.
280. Xu X, Toselli PA, Russell LD, Seldin DC. Globozoospermia in mice lacking the casein kinase II alpha' catalytic subunit. Nat Genet 1999;23:118-121.
281. Xu M, Xiao J, Chen J, Li J, Yin L, Zhu H, Zhou Z, Sha J. Identification and characterization of a novel human testis-specific Golgi protein, NYD-SP12. Mol Hum Reprod 2003; 9:9-17.
282. Yan W. Male infertility caused by spermiogenic defects: lessons from gene knockouts. Mol Cell Endocrinol 2009;306:24-32.
283. Yan X, Cao L, Li Q, Wu Y, Zhang H, Saiyin H, Liu X, Zhang X, Shi Q, Yu L. Aurora C is directly associated with Survivin and required for cytokinesis. Genes Cells 2005; 10:617-626.
284. Yang K-T, Li S-K, Chang C-C, Tang C-JC, Lin Y-N, Lee S-C, Tang TK. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 2010;21:2371-2383.
285. Yao R, Ito C, Natsume Y, Sugitani Y, Yamanaka H, Kuretake S, Yanagida K, Sato A, Toshimori K, Noda T. Lack of acrosome formation in mice lacking a Golgi protein, GOPC. Proc Natl Acad Sci USA 2002;99:11211-11216.
286. Yassine S, Escoffier J, Martinez G, Coutton C, Karaouzène T, Zouari R, Ravanat J-L, Metzler-Guillemain C, Fissore R, Hennebicq S et al. Dpy19l2-deficient globozoospermic sperm display altered genome packaging and DNA damage that compromises the initiation of embryo development. Mol Hum Reprod 2015a; 21:169-185.
287. Yassine S, Escoffier J, Nahed RA, Pierre V, Karaouzene T, Ray PF, Arnoult C. Dynamics of Sun5 localization during spermatogenesis in wild type and Dpy19l2 knock-out mice indicates that Sun5 is not involved in acrosome attachment to the nuclear envelope. PloS One 2015b;10:e0118698.
288. Yatsenko AN, O'Neil DS, Roy A, Arias-Mendoza PA, Chen R, Murthy LJ, Lamb DJ, Matzuk MM. Association of mutations in the zona pellucida binding protein 1 (ZPBP1) gene with abnormal sperm head morphology in infertile men. Mol Hum Reprod 2012;18:14-21.
289. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DMO, Hammer RE, Hamra FK, Matern S, Russell DW. Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest 2006; 116:2985-2994.
290. Yoon S-Y, Jellerette T, Salicioni AM, Lee HC, Yoo M-S, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE et al. Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. J Clin Invest 2008;118:3671-3681.
291. Yu Y, Fuscoe JC, Zhao C, Guo C, Jia M, Qing T, Bannon DI, Lancashire L, Bao W, Du T et al. Arat RNA-Seq transcriptomic Body Map across 11 organs and 4 developmental stages. Nat Commun 2014;5:3230.
292. Yurov YB, Saias MJ, Vorsanova SG, Erny R, Soloviev IV, Sharonin VO, Guichaoua MR, Luciani JM. Rapid chromosomal analysis of germ-line cells by FISH: an investigation of an infertile male with large-headed spermatozoa. Mol Hum Reprod 1996;2:665-668.
293. Zariwala MA, Knowles MR, Leigh MW. Primary ciliary dyskinesia. In: Pagon RA, Adam MP, Ardinger HH, Bird TD, Dolan CR, Fong C-T, Smith RJ, Stephens K (eds). Gene Reviewsw. Seattle, WA: University of Washington, Seattle, 1993. Available at: http://www.ncbi.nlm.nih.gov/books/NBK1122/. Accessed August 20, 2014.
294. Zariwala M, Noone PG, Sannuti A, Minnix S, Zhou Z, Leigh MW, Hazucha M, Carson JL, Knowles MR. Germline mutations in an intermediate chain dynein cause primary ciliary dyskinesia. Am J Respir Cell Mol Biol 2001;25:577-583.
295. Zariwala MA, Gee HY, Kurkowiak M, Al-Mutairi DA, Leigh MW, Hurd TW, Hjeij R, Dell SD, Chaki M, Dougherty GW et al. ZMYND10 is mutated in primary ciliary dyskinesia and interacts with LRRC6. Am J Hum Genet 2013;93:336-345.
296. Zekri A, Lesan V, Ghaffari SH, Tabrizi MH, Modarressi MH. Gene amplification and overexpression of Aurora-C in breast and prostate cancer cell lines. Oncol Res 2012;20:241-250.
297. Zhang Z, Kostetskii I, Moss SB, Jones BH, Ho C, Wang H, Kishida T, Gerton GL, Radice GL, Strauss JF. Haploinsufficiency for the murine orthologue of Chlamydomonas PF20 disrupts spermatogenesis. Proc Natl Acad Sci USA 2004; 101:12946-12951.
298. Zhang Z, Kostetskii I, Tang W, Haig-Ladewig L, Sapiro R, Wei Z, Patel AM, Bennett J, Gerton GL, Moss SB et al. Deficiency of SPAG16L causes male infertility associated with impaired sperm motility. Biol Reprod 2006;74:751-759.
299. Zhang F, Gu W, Hurles ME, Lupski JR. Copy number variation in human health, disease, and evolution. Annu Rev Genomics Hum Genet 2009;10:451-481.
300. Zhou J, Yao J, Joshi HC. Attachment and tension in the spindle assembly checkpoint. J Cell Sci 2002;115:3547-3555.
301. Zhu F, Gong F, Lin G, Lu G. DPY19L2 gene mutations are a major cause of globozoospermia: identification of three novel point mutations. Mol Hum Reprod 2013;19:395-404.