MNS1 is essential for spermiogenesis and motile ciliary functions in mice

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Zhou, Jian ^a   Yang, Fang ^a   Leu, N Adrian ^a   Wang, P Jeremy ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MNS1 PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; MNS1 PROTEIN, MOUSE; NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXONEME; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FLAGELLUM; GERM CELL; HYDROCEPHALUS; MALE; MALE STERILITY; MICROTUBULE; NONHUMAN; POLYMERIZATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SITUS INVERSUS; SOMATIC CELL; SPERMATOGENESIS; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; TRACHEA; ANIMAL; CELL CULTURE; CYTOLOGY; FERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PHYSIOLOGY; SPERMATID; SPERMATOZOON;

MUS;

ANIMALS; CELLS, CULTURED; CILIA; FERTILITY; GERM CELLS; HYDROCEPHALUS; MALE; MICE; NUCLEAR PROTEINS; SPERM TAIL; SPERMATIDS; SPERMATOGENESIS; SPERMATOZOA; TRACHEA;

EID: 84859233784     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002516     Document Type: Article

References (44)

1. Sharpe RM, (1993) Regulation of spermatogenesis. In: Knobil E, Neill JD, editors. The Physiology of Reproduction New York Raven Press pp. 1363-1434.
2. Eddy EM, O'Brien DA, (1993) The spermatozoon. In: Knobil E, Neill JD, editors. The Physiology of Reproduction New York Raven Press pp. 29-77.
3. Yanagimachi R, (1993) Mammalian fertilization. In: Knobil E, Neill JD, editors. The physiology of reproduction New York Raven Press pp. 189-317.
4. Chemes HE, Rawe VY, (2010) The making of abnormal spermatozoa: Cellular and molecular mechanisms underlying pathological spermiogenesis. Cell Tissue Res 341: 349-357.
5. Inglis PN, Boroevich KA, Leroux MR, (2006) Piecing together a ciliome. Trends Genet 22: 491-500.
6. Fliegauf M, Benzing T, Omran H, (2007) When cilia go bad: Cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8: 880-893.
7. Zariwala MA, Knowles MR, Omran H, (2007) Genetic defects in ciliary structure and function. Annu Rev Physiol 69: 423-450.
8. Ibanez-Tallon I, Pagenstecher A, Fliegauf M, Olbrich H, Kispert A, et al. (2004) Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet 13: 2133-2141.
9. Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, et al. (2002) Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 22: 6298-6305.
10. Sironen A, Kotaja N, Mulhern H, Wyatt TA, Sisson JH, et al. (2011) Loss of SPEF2 function in mice results in spermatogenesis defects and primary ciliary dyskinesia. Biol Reprod 85: 690-701.
11. Nonaka S, Shiratori H, Saijoh Y, Hamada H, (2002) Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418: 96-99.
12. McGrath J, Somlo S, Makova S, Tian X, Brueckner M, (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114: 61-73.
13. Pennarun G, Escudier E, Chapelin C, Bridoux AM, Cacheux V, et al. (1999) Loss-of-function mutations in a human gene related to chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 65: 1508-1519.
14. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, et al. (2011) The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 43: 79-84.
15. Merveille AC, Davis EE, Becker-Heck A, Legendre M, Amirav I, et al. (2011) 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 43: 72-78.
16. Lee L, Campagna DR, Pinkus JL, Mulhern H, Wyatt TA, et al. (2008) Primary ciliary dyskinesia in mice lacking the novel ciliary protein Pcdp1. Mol Cell Biol 28: 949-957.
17. Bartoloni L, Blouin JL, Pan Y, Gehrig C, Maiti AK, et al. (2002) 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 U S A 99: 10282-10286.
18. Ibanez-Tallon I, Gorokhova S, Heintz N, (2002) Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 11: 715-721.
19. Olbrich H, Haffner K, Kispert A, Volkel A, Volz A, et al. (2002) Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 30: 143-144.
20. Furukawa K, Inagaki H, Naruge T, Tabata S, Tomida T, et al. (1994) cDNA cloning and functional characterization of a meiosis-specific protein (MNS1) with apparent nuclear association. Chromosome Res 2: 99-113.
21. Carrera A, Moos J, Ning XP, Gerton GL, Tesarik J, et al. (1996) Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: Identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol 180: 284-296.
22. Cao W, Gerton GL, Moss SB, (2006) Proteomic profiling of accessory structures from the mouse sperm flagellum. Mol Cell Proteomics 5: 801-810.
23. Carrera A, Gerton GL, Moss SB, (1994) The major fibrous sheath polypeptide of mouse sperm: Structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 165: 272-284.
24. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, et al. (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426: 83-87.
25. Germino GG, (2005) Linking cilia to wnts. Nat Genet 37: 455-457.
26. Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, et al. (2002) A proteomic analysis of human cilia: Identification of novel components. Mol Cell Proteomics 1: 451-465.
27. Zhang Z, Shen X, Gude DR, Wilkinson BM, Justice MJ, et al. (2009) MEIG1 is essential for spermiogenesis in mice. Proc Natl Acad Sci U S A 106: 17055-17060.
28. Salzberg Y, Eldar T, Karminsky OD, Itach SB, Pietrokovski S, et al. (2010) Meig1 deficiency causes a severe defect in mouse spermatogenesis. Dev Biol 338: 158-167.
29. Lorenzetti D, Bishop CE, Justice MJ, (2004) Deletion of the parkin coregulated gene causes male sterility in the quaking(viable) mouse mutant. Proc Natl Acad Sci U S A 101: 8402-8407.
30. Bennett WI, Gall AM, Southard JL, Sidman RL, (1971) Abnormal spermiogenesis in quaking, a myelin-deficient mutant mouse. Biol Reprod 5: 30-58.
31. Sironen A, Thomsen B, Andersson M, Ahola V, Vilkki J, (2006) An intronic insertion in KPL2 results in aberrant splicing and causes the immotile short-tail sperm defect in the pig. Proc Natl Acad Sci U S A 103: 5006-5011.
32. Pazour GJ, Agrin N, Leszyk J, Witman GB, (2005) Proteomic analysis of a eukaryotic cilium. J Cell Biol 170: 103-113.
33. Stolc V, Samanta MP, Tongprasit W, Marshall WF, (2005) Genome-wide transcriptional analysis of flagellar regeneration in chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc Natl Acad Sci U S A 102: 3703-3707.
34. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, et al. (2004) Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117: 541-552.
35. Efimenko E, Bubb K, Mak HY, Holzman T, Leroux MR, et al. (2005) Analysis of xbx genes in C. elegans. Development 132: 1923-1934.
36. Blacque OE, Perens EA, Boroevich KA, Inglis PN, Li C, et al. (2005) Functional genomics of the cilium, a sensory organelle. Curr Biol 15: 935-941.
37. Ross AJ, Dailey LA, Brighton LE, Devlin RB, (2007) Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am J Respir Cell Mol Biol 37: 169-185.
38. Duriez B, Duquesnoy P, Escudier E, Bridoux AM, Escalier D, et al. (2007) A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc Natl Acad Sci U S A 104: 3336-3341.
39. Harlow E, Lane D, (1998) Using antibodies: A laboratory manual Cold Spring Harbor Cold Spring Harbor Laboratory Press.
40. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, et al. (2006) Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 173: 497-507.
41. Pan J, Goodheart M, Chuma S, Nakatsuji N, Page DC, et al. (2005) RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132: 4029-4039.
42. Zhou J, Pan J, Eckardt S, Leu NA, McLaughlin KJ, et al. (2011) Nxf3 is expressed in sertoli cells, but is dispensable for spermatogenesis. Mol Reprod Dev 78: 241-249.
43. Reddi PP, Naaby-Hansen S, Aguolnik I, Tsai JY, Silver LM, et al. (1995) Complementary deoxyribonucleic acid cloning and characterization of mSP-10: The mouse homologue of human acrosomal protein SP-10. Biol Reprod 53: 873-881.
44. Stanker LH, Wyrobek A, Balhorn R, (1987) Monoclonal antibodies to human protamines. Hybridoma 6: 293-303.