CoChat
Sign Up
Cited by 179Sperm and Testicular FunctionReproductive Biology and FertilityReproductive biology and impacts on aquatic species

Genetic abnormalities leading to qualitative defects of sperm morphology or function

Open access
Ray, P.F., Toure, A., Metzler‐Guillemain, C., Mitchell, M.J., Arnoult, C., Coutton, C.·2017·Clinical Genetics
DOI 10.1111/cge.12905
Open this paper in CoChat — free accountOpen PDF

Abstract

Infertility, defined by the inability of conceiving a child after 1 year is estimated to concern approximately 50 million couples worldwide. As the male gamete is readily accessible and can be studied by a simple spermogram it is easier to subcategorize male than female infertility. Subjects with a specific sperm phenotype are more likely to have a common origin thus facilitating the search for causal factors. Male infertility is believed to be often multifactorial and caused by both genetic and extrinsic factors, but severe cases of male infertility are likely to have a predominant genetic etiology. Patients presenting with a monomorphic teratozoospermia such as globozoospermia or macrospermia with more than 85% of the spermatozoa presenting this specific abnormality have been analyzed permitting to identify several key genes for spermatogenesis such as AURKC and DPY19L2. The study of patients with other specific sperm anomalies such as severe alteration of sperm motility, in particular multiple morphological anomalies of the sperm flagella (MMAF) or sperm unability to fertilize the oocyte (oocyte activation failure syndrome) has also enable the identification of new infertility genes. Here we review the recent works describing the identification and characterization of gene defects having a direct qualitative effect on sperm morphology or function.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/cge.12905

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Advances in the genetics of male infertility have shown a significant contribution of genetics towards abnormal sperm morphology, especially in cases of severe or specific sperm morphological defects.

    “Advances in the genetics of male infertility have shown a significant contribution of genetics towards abnormal sperm morphology (35), especially in cases of severe or specific sperm morphological defects (36).”

    From Isolated teratozoospermia: revisiting its relevance in male infertility: a narrative review (2024) · cites this paper as [36]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 99

  1. Mascarenhas MN, Flaxman SR, Boerma T, Vanderpoel S, Stevens GA. National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys. PLoS Med 2012: 9 (12): e1001356.
  2. Benzacken B, Gavelle FM, Martin-Pont B et al. Familial sperm poly- ploidy induced by genetic spermatogenesis failure: case report. Hum Reprod 2001: 16 (12): 2646-2651.
  3. Escalier D. Human spermatozoa with large heads and multiple flagella: a quantitative ultrastructural study of 6 cases. Biol Cell 1983: 48 (1): 65-74.
  4. Devillard F, Metzler-Guillemain C, Pelletier R et al. Polyploidy in large-headed sperm: FISH study of three cases. Hum Reprod 2002: 17 (5): 1292-1298.
  5. Nistal M, Paniagua R, Herruzo A. Multi-tailed spermatozoa in a case with asthenospermia and teratospermia. Virchows Arch B Cell Pathol 1977: 26 (2): 111-118.
  6. 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 (2): 130-135.
  7. Achard V, Paulmyer-Lacroix O, Mercier G et al. Reproductive failure in patients with various percentages of macronuclear spermatozoa: high level of aneuploid and polyploid spermatozoa. J Androl 2007: 28 (4): 600-606.
  8. Vicari E, De PA, Burrello N et al. Absolute polymorphic teratozoosper- mia in patients with oligo-asthenozoospermia is associated with an ele- vated sperm aneuploidy rate. J Androl 2003: 24 (4): 598-603.
  9. Dieterich K, Soto RR, Faure AK et al. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet 2007: 39 (5): 661-665.
  10. Ben Khelifa M, Zouari R, Harbuz R et al. A new AURKC mutation causing macrozoospermia: implications for human spermatogenesis and clinical diagnosis. Mol Hum Reprod 2011: 17 (12): 762-768.
  11. Yang KT, Li SK, Chang CC et al. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 2010: 21 (14): 2371-2383.
  12. Tang CJ, Lin CY, Tang TK. Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol 2006: 290 (2): 398-410.
  13. Assou S, Anahory T, Pantesco V et al. The human cumulus -oocyte complex gene-expression profile. Hum Reprod 2006: 21 (7): 1705-1719.
  14. 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 (3): 406-409.
  15. Chen HL, Tang CJ, Chen CY, Tang TK. Overexpression of an Aurora-C kinase-deficient mutant disrupts the Aurora-B/INCENP complex and induces polyploidy. J Biomed Sci 2005: 12 (2): 297-310.
  16. Vagnarelli P, Earnshaw WC. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 2004: 113 (5): 211-222.
  17. van der Horst A, Lens SM. Cell division: control of the chromosomal passenger complex in time and space. Chromosoma 2014: 123 (1-2): 25-42.
  18. Carmena M, Wheelock M, Funabiki H, Earnshaw WC. The chromo- somal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 2012: 13 (12): 789-803.
  19. Yan X, Cao L, Li Q et al. Aurora C is directly associated with Survivin and required for cytokinesis. Genes Cells 2005: 10 (6): 617-626.
  20. Kimmins S, Crosio C, Kotaja N et al. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 2007: 21 (3): 726-739.
  21. 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 (33): E2215-E2222.
  22. 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 (2): e1004194.
  23. Dieterich K, Zouari R, Harbuz R 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 (7): 1301-1309.
  24. Fellmeth JE, Gordon D, Robins CE, Scott RT Jr, Treff NR, Schindler K. Expression and characterization of three Aurora kinase C splice variants found in human oocytes. Mol Hum Reprod 2015: 21 (8): 633-644.
  25. Chianese C, Fino MG, Riera EA et al. Comprehensive investigation in patients affected by sperm macrocephaly and globozoospermia. Andrology 2015: 3 (2): 203-212.
  26. Ghedir H, Gribaa M, Mamai O et al. Macrozoospermia: screening for the homozygous c.144delC mutation in AURKC gene in infertile men and estimation of its heterozygosity frequency in the Tunisian population. J Assist Reprod Genet 2015: 32 (11): 1651-1658.
  27. Ounis L, Zoghmar A, Coutton 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 (1): 68-73.
  28. Ben KM, Coutton C, Blum MG et al. Identification of a new recurrent aurora kinase C mutation in both European and African men with macrozoospermia. Hum Reprod 2012: 27 (11): 3337-3346.
  29. Aarabi M, Yu Y, Xu W et al. The testicular and epididymal expression profile of PLCzeta in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS One 2012: 7 (3): e33496.
  30. Eloualid A, Rouba H, Rhaissi H et al. Prevalence of the Aurora kinase C c.144delC mutation in infertile Moroccan men. Fertil Steril 2014: 101 (4): 1086-1090.
  31. El KF, Lamzouri A, Laarabi FZ, Zahi M, Ben AB, Sefiani A. Confir- mation of the high prevalence in Morocco of the homozygous mutation c.144delC in the aurora kinase C gene (AURKC) in the teratozoosper- mia with large-headed spermatozoa. J Gynecol Obstet Biol Reprod (Paris) 2011: 40 (4): 329-333.
  32. Molinari E, Mirabelli M, Raimondo S et al. Sperm macrocephaly syndrome in a patient without AURKC mutations and with a history of recurrent miscarriage. Reprod Biomed Online 2013: 26 (2): 148-156.
  33. Coutton C, Escoffier J, Martinez G, Arnoult C, Ray PF. Teratozoosper- mia: spotlight on the main genetic actors in the human. Hum Reprod Update 2015: 21 (4): 455-485.
  34. Chelli MH, Albert M, Ray PF et al. Can intracytoplasmic morpholog- ically selected sperm injection be used to select normal-sized sperm heads in infertile patients with macrocephalic sperm head syndrome? Fertil Steril 2010: 93 (4): 1347.e1-5.
  35. Kahraman S, Akarsu C, Cengiz G et al. Fertility of ejaculated and tes- ticular megalohead spermatozoa with intracytoplasmic sperm injection. Hum Reprod 1999: 14 (3): 726-730.
  36. Dam AH, Feenstra I, Westphal JR, Ramos L, van Golde RJ, Kremer JA. Globozoospermia revisited. Hum Reprod Update 2007: 13 (1): 63-75.
  37. Holstein AF, Schirren C, Schirren CG. Human spermatids and sperma- tozoa lacking acrosomes. J Reprod Fertil 1973: 35 (3): 489-491.
  38. Sen CGS, Holstein AF, Schirren C. Uber die Morphogenese rundkop- figer Spermatozoen des Menschen. Andrologie 1971: 3 (3): 117-25.
  39. Dam AH, Ramos L, Dijkman HB et al. Morphology of partial globo- zoospermia. J Androl 2011: 32 (2): 199-206.
  40. Dirican EK, Isik A, Vicdan K, Sozen E, Suludere Z. Clinical preg- nancies 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 (2): 332-336.
  41. Kilani Z, Ismail R, Ghunaim S et al. Evaluation and treatment of familial globozoospermia in five brothers. Fertil Steril 2004: 82 (5): 1436-1439.
  42. Dale B, Iaccarino M, Fortunato A, Gragnaniello G, Kyozuka K, Tosti E. A morphological and functional study of fusibility in round-headed spermatozoa in the human. Fertil Steril 1994: 61 (2): 336-340.
  43. Florke-Gerloff S, Topfer-Petersen E, Muller-Esterl W et al. Biochemi- cal and genetic investigation of round-headed spermatozoa in infertile men including two brothers and their father. Andrologia 1984: 16 (3): 187-202.
  44. Kullander S, Rausing A. On round-headed human spermatozoa. Int J Fertil 1975: 20 (1): 33-40.
  45. Yatsenko AN, O'Neil DS, Roy A et al. 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 (1): 14-21.
  46. Liu G, Shi QW, Lu GX. A newly discovered mutation in PICK1 in a human with globozoospermia. Asian J Androl 2010: 12 (4): 556-560.
  47. Dam AH, Koscinski I, Kremer JA et al. Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. Am J Hum Genet 2007: 81 (4): 813-820.
  48. Lu L, Lin M, Xu M, Zhou ZM, Sha JH. Gene functional research using polyethylenimine-mediated in vivo gene transfection into mouse spermatogenic cells. Asian J Androl 2006: 8 (1): 53-59.
  49. Elinati E, Fossard C, Okutman O et al. A new mutation identified in SPATA16 in two globozoospermic patients. J Assist Reprod Genet 2016: 33 (6): 815-820.
  50. 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 (1): 103-107.
  51. Harbuz R, Zouari R, Pierre V 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 (3): 351-361.
  52. Pierre V, Martinez G, Coutton C et al. 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 (16): 2955-2965.
  53. Koscinski I, Elinati E, Fossard C, Redin C, Muller J. Velez dlC et al. DPY19L2 deletion as a major cause of globozoospermia. Am J Hum Genet 2011: 88 (3): 344-350.
  54. Coutton C, Zouari R, Abada F et al. MLPA and sequence analysis of DPY19L2 reveals point mutations causing globozoospermia. Hum Reprod 2012: 27 (8): 2549-2558.
  55. Elinati E, Kuentz P, Redin C et al. Globozoospermia is mainly due to DPY19L2 deletion via non-allelic homologous recombination involv- ing two recombination hotspots. Hum Mol Genet 2012: 21 (16): 3695-3702.
  56. Ghedir H, Ibala-Romdhane S, Okutman O, Viot G, Saad A, Viville S. Identification of a new DPY19L2 mutation and a better definition of DPY19L2 deletion breakpoints leading to globozoospermia. Mol Hum Reprod 2016: 22 (1): 35-45.
  57. 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 (6): 395-404.
  58. 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, Balkan. J Med Genet 2013: 16 (1): 73-76.
  59. Coutton C, Abada F, Karaouzene T et al. 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 (3): e1003363.
  60. Liu P, Carvalho CM, Hastings PJ, Lupski JR. Mechanisms for recurrent and complex human genomic rearrangements. Curr Opin Genet Dev 2012: 22 (3): 211-220.
  61. Buettner FF, Ashikov A, Tiemann B, Lehle L, Bakker H. C. elegans DPY-19 is a C-mannosyltransferase glycosylating thrombospondin repeats. Mol Cell 2013: 50 (2): 295-302.
  62. Davila 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 (3): 229-246.
  63. Kashir J, Heindryckx B, Jones C, De SP, Parrington J, Coward K. Oocyte activation, phospholipase C zeta and human infertility. Hum Reprod Update 2010: 16 (6): 690-703.
  64. Escoffier J, Lee HC, Yassine S et al. Homozygous mutation of PLCZ1 leads to defective human oocyte activation and infertility that is not res- cued by the WW-binding protein PAWP. Hum Mol Genet 2015: 25 (5): 878-891.
  65. Escoffier J, Yassine S, Lee HC et al. Subcellular localization of phos- pholipase Czeta in human sperm and its absence in DPY19L2-deficient sperm are consistent with its role in oocyte activation. Mol Hum Reprod 2015: 21 (2): 157-168.
  66. Amdani SN, Jones C, Coward K. Phospholipase C zeta (PLCzeta): oocyte activation and clinical links to male factor infertility. Adv Biol Regul 2013: 53 (3): 292-308.
  67. Heytens E, Parrington J, Coward K et al. Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod 2009: 24 (10): 2417-2428.
  68. Yoon SY, Jellerette T, Salicioni AM 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 (11): 3671-3681.
  69. Yassine S, Escoffier J, Martinez G et al. Dpy19l2-deficient globo- zoospermic sperm display altered genome packaging and DNA dam- age that compromises the initiation of embryo development. Mol Hum Reprod 2015: 21 (2): 169-185.
  70. Brahem S, Mehdi M, Elghezal H, Saad A. Detection of DNA fragmen- tation and meiotic segregation in human with isolated teratozoospermia. J Assist Reprod Genet 2011: 28 (1): 41-48.
  71. Perrin A, Coat C, Nguyen MH et al. Molecular cytogenetic and genetic aspects of globozoospermia: a review. Andrologia 2013: 45 (1): 1-9.
  72. Chemes HE, Carizza C, Scarinci F, Brugo 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 (2): 310-316.
  73. Chemes HE, Rawe VY. The making of abnormal spermatozoa: cellular and molecular mechanisms underlying pathological spermiogenesis. Cell Tissue Res 2010: 341 (3): 349-357.
  74. Le LD. Teratospermia consisting of the absence of the head of the spermatozoa because of a fault in the joint between the head and the neck of the sperm in man (author's transl). J Gynecol Obstet Biol Reprod (Paris) 1979: 8 (1): 43-45.
  75. 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 (5): 1787.e19-23.
  76. Panidis D, Rousso D, Kourtis A, Gianoulis C, Papathanasiou K, Kalachanis J. Headless spermatozoa in semen specimens from fertile and subfertile men. J Reprod Med 2001: 46 (11): 947-950.
  77. Perotti ME, Giarola A, Gioria M. Ultrastructural study of the decap- itated sperm defect in an infertile man. J Reprod Fertil 1981: 63 (2): 543-549.
  78. Perotti ME, Gioria M. Fine structure and morphogenesis of "headless" human spermatozoa associated with infertility. Cell Biol Int Rep 1981: 5 (2): 113.
  79. 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 (2): 109-115.
  80. Zhu F, Wang F, Yang X et al. Biallelic sun5 mutations cause autosomal-recessive acephalic spermatozoa syndrome. Am J Hum Genet 2016: 99 (4): 942-949.
  81. Yassine S, Escoffier J, Nahed RA et al. 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 2015: 10 (3): e0118698.
  82. Yuan S, Stratton CJ, Bao J 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 (5): E430-E439.
  83. Brown JM, Witman GB. Cilia and diseases. Bioscience 2014: 64 (12): 1126-1137.
  84. Bisgrove BW, Yost HJ. The roles of cilia in developmental disorders and disease. Development 2006: 133 (21): 4131-4143.
  85. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002: 53 (1-2): 133-150.
  86. Xie F, Garcia MA, Carlson AE et al. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Dev Biol 2006: 296 (2): 353-362.
  87. Jaiswal BS, Conti M. Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc Natl Acad Sci USA 2003: 100 (19): 10676-10681.
  88. Cooper TG, Noonan E, von ES et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update 2010: 16 (3): 231-245.
  89. Horani A, Brody SL, Ferkol TW. Picking up speed: advances in the genetics of primary ciliary dyskinesia. Pediatr Res 2014: 75 (1-2): 158-164.
  90. Ben Khelifa M, Coutton C, Zouari R 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 (1): 95-104.
  91. 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 (10): 2790-2794.
  92. 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 (5): 405-428. 100. Yang SM, Li HB, Wang JX et al. Morphological characteristics and initial genetic study of multiple morphological anomalies of the flagella in China. Asian J Androl 2015: 17 (3): 513-515. 101. Ben KM, Coutton C, Zouari R 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 (1): 95-104. 102. Neesen J, Kirschner R, Ochs M et al. Disruption of an inner arm dynein heavy chain gene results in asthenozoospermia and reduced ciliary beat frequency. Hum Mol Genet 2001: 10 (11): 1117-1128. 103. Amiri-Yekta A, Coutton C, Kherraf ZE et al. Whole-exome sequencing of familial cases of multiple morphological abnormalities of the sperm flagella (MMAF) reveals new DNAH1 mutations. Hum Reprod 2016. doi: 10.1093. 104. Wang X, Jin H, Han F et al. Homozygous DNAH1 frame-shift muta- tion causes multiple morphological anomalies of the sperm flagella (MMAF) in Chinese. Clin Genet 2016. 105.
  93. Imtiaz F, Allam R, Ramzan K, Al-Sayed M. Variation in DNAH1 may contribute to primary ciliary dyskinesia. BMC Med Genet 2015: 16: 14. 106. Wambergue C, Zouari R, Fourati Ben MS et al. Patients with multiple morphological abnormalities of the sperm flagella due to DNAH1 mutations have a good prognosis following intracytoplasmic sperm injection. Hum Reprod 2016: 31 (6): 1164-1172. 107. Coutton C, Arnoult C, Ray PF. Commentary on "morphological characteristics and initial genetic study of multiple morphological anomalies of the flagella in China". Asian J Androl 2016: 18 (5): 812. 108. Kuo YC, Shen YR, Chen HI et al. SEPT12 orchestrates the formation of mammalian sperm annulus by organizing core octameric complexes with other SEPT proteins. J Cell Sci 2015: 128 (5): 923-934. 109. Ihara M, Kinoshita A, Yamada S et al. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell 2005: 8 (3): 343-352. 110.
  94. Kissel H, Georgescu MM, Larisch S, Manova K, Hunnicutt GR, Steller H. The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell 2005: 8 (3): 353-364. 111. Lin YH, Lin YM, Wang YY et al. The expression level of septin12 is critical for spermiogenesis. Am J Pathol 2009: 174 (5): 1857-1868. 112. Kuo PL, Chiang HS, Wang YY et al. SEPT12-microtubule complexes are required for sperm head and tail formation. Int J Mol Sci 2013: 14 (11): 22102-22116. 113. Lhuillier P, Rode B, Escalier D et al. Absence of annulus in human asthenozoospermia: case report. Hum Reprod 2009: 24 (6): 1296-1303. 114. Sugino Y, Ichioka K, Soda T et al. Septins as diagnostic markers for a subset of human asthenozoospermia. J Urol 2008: 180 (6): 2706-2709. 115. Dirami T, Rode B, Wolf JP, Gacon G, Dulioust E, Toure A. Assessment of the frequency of sperm annulus defects in a large cohort of patients presenting asthenozoospermia. Basic Clin Androl 2015: 25: 10. 116.
  95. Hosseinifar H, Shafipour M, Modarresi T et al. Relationship between absence of annulus and asthenozoospermia in Iranian men. J Assist Reprod Genet 2014: 31 (12): 1681-1685. 117. Kuo YC, Lin YH, Chen HI et al. SEPT12 mutations cause male infertility with defective sperm annulus. Hum Mutat 2012: 33 (4): 710-719. 118. Singh AP, Rajender S. CatSper channel, sperm function and male fertility. Reprod Biomed Online 2015: 30 (1): 28-38. 119. Hildebrand MS, Avenarius MR, Fellous M et al. Genetic male infertility and mutation of CATSPER ion channels. Eur J Hum Genet 2010: 18 (11): 1178-1184. 120. Ren D, Navarro B, Perez G et al. A sperm ion channel required for sperm motility and male fertility. Nature 2001: 413 (6856): 603-609. 121. Lishko PV, Botchkina IL, Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature 2011: 471 (7338): 387-391. 122. Strunker T, Goodwin N, Brenker C et al. The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 2011: 471 (7338): 382-386. 123. Chung JJ, Navarro B, Krapivinsky G, Krapivinsky L, Clapham DE. A novel gene required for male fertility and functional CATSPER channel formation in spermatozoa. Nat Commun 2011: 2: 153. 124. Qi H, Moran MM, Navarro B et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci USA 2007: 104 (4): 1219-1223. 125. Carlson AE, Quill TA, Westenbroek RE, Schuh SM, Hille B, Babcock DF. Identical phenotypes of CatSper1 and CatSper2 null sperm. J Biol Chem 2005: 280 (37): 32238-32244. 126. Avenarius MR, Hildebrand MS, Zhang Y et al. Human male infertility caused by mutations in the CATSPER1 channel protein. Am J Hum Genet 2009: 84 (4): 505-510. 127. Zhang Y, Malekpour M, Al-Madani N et al. Sensorineural deafness and male infertility: a contiguous gene deletion syndrome. J Med Genet 2007: 44 (4): 233-240. 128. Avidan N, Tamary H, Dgany O et al. CATSPER2, a human autosomal nonsyndromic male infertility gene. Eur J Hum Genet 2003: 11 (7): 497-502. 129. Shukla KK, Mahdi AA, Rajender S. Ion channels in sperm physiology and male fertility and infertility. J Androl 2012: 33 (5): 777-788. 130.
  96. Toure A, Morin L, Pineau C, Becq F, Dorseuil O, Gacon G. Tat1, a novel sulfate transporter specifically expressed in human male germ cells and potentially linked to rhogtpase signaling. J Biol Chem 2001: 276 (23): 20309-20315. 131
  97. Toure A, Lhuillier P, Gossen JA et al. The testis anion transporter 1 (Slc26a8) is required for sperm terminal differentiation and male fertility in the mouse. Hum Mol Genet 2007: 16 (15): 1783-1793. 132. Rode B, Dirami T, Bakouh N et al. The testis anion transporter TAT1 (SLC26A8) physically and functionally interacts with the cystic fibrosis transmembrane conductance regulator channel: a potential role during sperm capacitation. Hum Mol Genet 2012: 21 (6): 1287-1298. 133. Mount DB, Romero MF. The SLC26 gene family of multifunctional anion exchangers. Pflugers Arch 2004: 447 (5): 710-721. 134. Avella M, Loriol C, Boulukos K, Borgese F, Ehrenfeld J. SLC26A9 stimulates CFTR expression and function in human bronchial cell lines. J Cell Physiol 2011: 226 (1): 212-223. 135. Homma K, Miller KK, Anderson CT et al. Interaction between CFTR and prestin (SLC26A5). Biochim Biophys Acta 2010: 1798 (6): 1029-1040. 136. Singh AK, Riederer B, Chen M et al. The switch of intestinal Slc26 exchangers from anion absorptive to HCOFormula secretory mode is dependent on CFTR anion channel function. Am J Physiol Cell Physiol 2010: 298 (5): C1057-C1065. 137.
  98. Shcheynikov N, Wang Y, Park M et al. Coupling modes and stoichiom- etry of Cl-/. J Gen Physiol 2006: 127 (5): 511-524. 138. Bertrand CA, Zhang R, Pilewski JM, Frizzell RA. SLC26A9 is a constitutively active, CFTR-regulated anion conductance in human bronchial epithelia. J Gen Physiol 2009: 133 (4): 421-438. 139. Chang MH, Plata C, Sindic A et al. Slc26a9 is inhibited by the R-region of the cystic fibrosis transmembrane conductance regulator via the STAS domain. J Biol Chem 2009: 284 (41): 28306-28318. 140. Ko SB, Zeng W, Dorwart MR et al. Gating of CFTR by the STAS domain of SLC26 transporters. Nat Cell Biol 2004: 6 (4): 343-350. 141. Hernandez-Gonzalez EO, Trevino CL, Castellano LE et al. Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation. J Biol Chem 2007: 282 (33): 24397-24406. 142. Xu WM, Shi QX, Chen WY et al. Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility. Proc Natl Acad Sci USA 2007: 104 (23): 9816-9821. 143. Figueiras-Fierro D, Acevedo JJ, Martinez-Lopez P et al. Electrophys- iological evidence for the presence of cystic fibrosis transmembrane conductance regulator (CFTR) in mouse sperm. J Cell Physiol 2013: 228 (3): 590-601. 144. Escoffier J, Krapf D, Navarrete F, Darszon A, Visconti PE. Flow cytometry analysis reveals a decrease in intracellular sodium during sperm capacitation. J Cell Sci 2012: 125 (Pt 2): 473-485. 145. Dirami T, Rode B, Jollivet M et al. Missense mutations in SLC26A8, encoding a sperm-specific activator of CFTR, are associated with human asthenozoospermia. Am J Hum Genet 2013: 92 (5): 760-766. 146.
  99. Toure A, Rode B, Hunnicutt GR, Escalier D, Gacon G. Septins at the annulus of mammalian sperm. Biol Chem 2011: 392 (8-9): 799-803. 147. Nomikos M, Kashir J, Swann K, Lai FA. Sperm PLCzeta: from structure to Ca2+ oscillations, egg activation and therapeutic potential. FEBS Lett 2013: 587 (22): 3609-3616. 148. Chithiwala ZH, Lee HC, Hill DL et al. Phospholipase C-zeta deficiency as a cause for repetitive oocyte fertilization failure during ovarian stimulation for in vitro fertilization with ICSI: a case report. J Assist Reprod Genet 2015: 32 (9): 1415-1419. 149. Kashir J, Konstantinidis M, Jones C et al. A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCzeta) leads to male infertility. Hum Reprod 2012: 27 (1): 222-231. 150. Escoffier J, Lee HC, Yassine S et al. Homozygous mutation of PLCZ1 leads to defective human oocyte activation and infertility that is not rescued by the WW-binding protein PAWP. Hum Mol Genet 2016: 25 (5): 878-891. 151. Carlson AE, Westenbroek RE, Quill T et al. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci USA 2003: 100 (25): 14864-14868. 152. Quill TA, Sugden SA, Rossi KL, Doolittle LK, Hammer RE, Gar- bers DL. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc Natl Acad Sci USA 2003: 100 (25): 14869-14874.

Cited by

Sorted by citations

Authors
Ray, P. F., Toure, A., Metzler‐Guillemain, C., Mitchell, M. J., Arnoult, C., & Coutton, C.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Institut Cochin INSERM U1016 Paris France
  • Inserm (FR)
Corresponding author
Ray, P.F.
ORCID
Venue
Clinical Genetics
Publisher
Wiley
Published
2016-12-09
Volume
91
Issue
2
Pages
217-232
ISSN
  • 0009-9163 (ISSN-L)
  • 1399-0004
DOI
10.1111/cge.12905
OpenAlex
W2533955468
Cited by
179
References
3
Citations by year
2026: 8 · 2025: 16 · 2024: 19 · 2023: 10 · 2022: 16 · 2021: 25 · 2020: 23 · 2019: 32 · 2018: 23 · 2017: 6 · 2012: 1
FWCI
2.92
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Clinical Genetics (publishedVersion)
  • PubMed (publishedVersion)
Funders
ANR/DGOS funded PRTS project MAS-FLAGELLA
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
male infertility, sperm morphology, sperm function, teratozoospermia, globozoospermia, AURKC, DPY19L2, spermatogenesis genes
MeSH terms
Teratozoospermia, Female, Humans, Infertility, Male, Male, Membrane Proteins, Oocytes, Sperm Motility, Sperm Tail, Spermatogenesis, Spermatozoa, Aurora Kinase C

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review