Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Milani, Liliana ^a   Ghiselli, Fabrizio ^a   Maurizii, Maria Gabriella ^a   Passamonti, Marco ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; DEAD BOX PROTEIN VASA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BALBIANI BODY; BIOLOGICAL MODEL; CELL AGGREGATION; CELL DIVISION; CELL ORGANELLE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CHROMATOID BODY; CLAM; CONTROLLED STUDY; DOUBLY UNIPARENTAL INHERITANCE; EMBRYO; FEMALE; GAMETE; GERM LINE; GONAD DEVELOPMENT; IMMUNOCYTOCHEMISTRY; IMMUNOLOCALIZATION; INHERITANCE; MALE; MICROTUBULE; MITOCHONDRION; MITOSIS SPINDLE; MOLECULAR DYNAMICS; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; RUDITAPES PHILIPPINARUM; SPERMATOZOON; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; BIVALVIA; CHROMOSOME SEGREGATION; DEAD-BOX RNA HELICASES; EMBRYO, NONMAMMALIAN; FEMALE; GONADS; INHERITANCE PATTERNS; MALE; MICROTUBULES; MITOCHONDRIA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPERMATOZOA;

EID: 82255162357     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028194     Document Type: Article

References (108)

1. Eddy EM, (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43: 229-281.
2. Illmensee K, Mahowald AP, Loomis MR, (1976) The ontogeny of germ plasm during oogenesis in Drosophila. Dev Biol 49: 40-65.
3. Rongo C, Lehmann R, (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm, Trends Genet 12: 102-109.
4. Ikenishi K, (1998) Germ Plasm in Caenorhabditis elegans, Drosophila and Xenopus. Develop. Growth Differ 40: 1-10.
5. Saffman EE, Lasko P, (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55: 1141-1163.
6. Wylie C, (1999) Germ cells. Cell 96: 165-174.
7. Matova N, Cooley L, (2001) Comparative Aspects of Animal Oogenesis. Dev Biol 231: 291-320.
8. Becalska AN, Gavis EG, (2010) Bazooka regulates microtubule organization and spatial restriction of germ plasm assembly in the Drosophila oocyte. Dev Biol 340: 528-538.
9. Kloc M, Bilinski S, Chan AP, Allen LH, Zearfoss NR, et al. (2001) RNA localization and germ cell determination in Xenopus. Int Rev Cytol 203: 63-91.
10. Kloc M, Bilinski S, Etkin LD, (2004) The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59: 1-36.
11. Kloc M, Etkin LD, (2005) RNA localization mechanisms in oocytes. J Cell Sci 118: 269-282.
12. Hay B, Ackerman L, Barbel S, Jan LY, Jan YN, (1988) Identification of a component of Drosophila polar granules. Development 103: 625-640.
13. Hay B, Jan LY, Jan YN, (1988) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55: 577-587.
14. Gustafson EA, Wessel GM, (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32: 626-637.
15. Lasko F, Ashburner M, (1988) The product of the Drosophila gene vasa is very similar to eucaryotic initiation factor-4A. Nature 335: 611-617.
16. Williamson A, Lehmann R, (1996) Germ Cell Development in Drosophila. Annu Rev Devel Biol 12: 365-391.
17. Knaut H, Pelegri F, Bohmann K, Schwarz H, Nuesslein-Volhard C, (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J Cell Biol 149: 875-888.
18. Kuznicki KA, Smith PA, Leung-Chiu WM, Estevez AO, Scott HC, et al. (2000) Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127: 2907-2916.
19. Raz E, (2000) The function and regulation of vasa-like genes in germ-cell development. Genome Biol 1: REVIEWS1017.1-1017.6.
20. Reunov A, (2006) Structures related to the germ plasm in mouse. Zygote 14: 231-238.
21. Cox RT, Spradling AC, (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130: 1579-1590.
22. Russell L, Frank B, (1978) Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat Rec 190: 79-97.
23. Parvinen M, (2005) The chromatoid body in spermatogenesis. Int J Androl 28: 189-201.
24. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, et al. (2006) The chromatoid body of male germ cells: Similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 103: 2647-2652.
25. Kotaja N, Sassone-Corsi P, (2007) The chromatoid body: a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Bio 8: 85-90.
26. Shang P, Baarends WM, Hoogerbrugge J, Ooms MP, van Cappellen WA, et al. (2010) Functional transformation of the chromatoid body in mouse spermatids requires testis-specific serine/threonine kinases. J Cell Sci 123: 331-339.
27. Kobayashi S, Amikura R, Okada M, (1993) Presence of Mitochondrial Large Ribosomal RNA Outside Mitochondria in Germ Plasm of Drosophila melanogaster. Science 260: 1521-1524.
28. Ding D, Whittaker KL, Lipshitz HD, (1994) Mitochondrially Encoded 16S Large Ribosomal RNA is Concentrated in the Posterior Polar Plasm of Early Drosophila Embryos but is not Required for Pole Cell Formation. Dev Biol 163: 503-515.
29. Iida T, Kobayashi S, (1998) Essential role of mitochondrially encoded large rRNA for germ-line formation in Drosophila embryos. Proc Natl Acad Sci U S A 95: 11274-11278.
30. Kobayashi S, Amikura R, Mukai M, (1998) Localization of Mitochondrial RNA in Germ Plasm of Xenopus Embryos. Curr Biol 8: 1117-1120.
31. Ogawa M, Amikura R, Akasaka K, Kinoshita T, Kobayashi S, et al. (1999) Asymmetrical Distribution of Mitochondrial rRNA into Small Micromeres of Sea Urchin Embryos. Zool Sci 16: 445-451.
32. Amikura R, Kashikawa, M, Nakamura A, Kobayashi S, (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci U S A 98: 9133-9138.
33. Reunov A, Isaeva V, Au D, Wu R, (2000) Nuage constituents arising from mitochondria: Is it possible? Develop Growth Differ 42: 139-143.
34. Isaeva VV, Reunov AA, (2001) Germ Plasm and Germ-line Cell Determination: The Role of Mitochondria. Russ J Mar Biol 27: S8-S14.
35. Amikura R, Sato K, Kobayashi S, (2005) Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mech Develop 122: 1087-1093.
36. Andersson SGE, Zomorodipour A, Andersson JO, Sicheritz-Pontén T, Alsmark UCM, et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of Mitochondria. Nature 396: 133-143.
37. Ebbert MA, (1993) Endosymbiotic sex ratio distorters in insects and mites. In: Wrensh DL, Ebbert MA, editors. Evolution and Diversity of Sex Ratio in Insects and Mites New York Chapman Hall pp. 150-191.
38. Hurst GDD, Hurst LD, Majerus MEN, (1997) Cytoplasmic sex-ratio distorters. In: O'Neil SL, Hoffmann AA, Werren JH, editors. Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction UK Oxford University Press pp. 125-154.
39. Negri I, Franchini A, Gonella E, Daffonchio D, Mazzoglio PJ, et al. (2009) Unravelling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting. Proc R Soc B 276: 2485-2491.
40. Smiraglia DJ, Kulawiec M, Bistulfi GL, Gupta SG, Singh KK, (2008) A novel role for mitochondria in regulating epigenetic modification in the nucleus. Cancer Biol Ther 7: 1182-1190.
41. Cao L, Shitara H, Horii T, Nagao Y, Imai H, et al. (2007) The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet 39: 386-390.
42. Shoubridge EA, Wai T, (2007) Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol 77: 87-111.
43. Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P, et al. (2008) A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 40: 249-254.
44. Tourte M, Mignotte F, Mounolou JC, (1984) Heterogeneous distribution and replication activity of mitochondria in Xenopus laevis oocytes. Eur J Cell Biol 34: 171-178.
45. Mignotte F, Tourte M, Mounolou JC, (1987) Segregation of mitochondria in the cytoplasm of Xenopus vitellogenic oocytes. Cell 60: 97-102.
46. Volodina N, Denegre JM, Mowry KL, (2003) Apparent Mitochondrial Asymmetry in Xenopus Eggs. Dev Dynam 226: 654-662.
47. Zhou RR, Wang B, Wang J, Schatten H, Zhang YZ, (2010) Is the mitochondrial cloud the selection machinery for preferentially transmitting wild-type mtDNA between generations? Rewinding Müller's ratchet efficiently. Curr Genet 56: 101-107.
48. Chuma S, Hosokawa M, Tanaka T, Nakatsuji N, (2009) Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol Cell Endocrinol 306: 17-23.
49. Obata M, Komaru A, (2005) Specific location of sperm mitochondria in mussel Mytilus galloprovincialis zygotes stained by MitoTracker. Dev Growth Differ 47: 255-263.
50. Katayama M, Zhong Z, Lai L, Sutovsky P, Prather RS, et al. (2006) Mitochondrial distribution and microtubule organization in fertilized and cloned porcine embryos: Implications for developmental potential. Dev Biol 299: 206-220.
51. Zhang YZ, Ouyang YC, Hou Y, Schatten H, Chen DY, et al. (2008) Mitochondrial behavior during oogenesis in zebrafish: A confocal microscopy analysis. Develop Growth Differ 50: 189-201.
52. Breton S, Beaupre HD, Stewart DT, Hoeh WR, Blier PU, (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn't one enough? Trends Genet 23: 465-474.
53. Passamonti M, Ghiselli F, (2009) Doubly Uniparental Inheritance: Two Mitochondrial Genomes, One Precious Model for Organelle DNA Inheritance and Evolution. (Review). DNA Cell Biol 28: 79-89.
54. Kaneda H, Hayashi J, Takahama S, Taya C, Fischer Lindhal K, et al. (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci U S A 92: 4542-4546.
55. Shitara H, Hayashi JI, Takahama S, Kaneda H, Yonekawa H, (1998) Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage. Genetics 148: 851-857.
56. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, et al. (1999) Ubiquitin tag for sperm mitochondria. Nature 402: 371-372.
57. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, et al. (2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63: 582-590.
58. Theologidis I, Fodelianakis S, Gaspar MB, Zouros E, (2008) Doubly uniparental inheritance (DUI) of mitochondrial DNA in Donax trunculus (Bivalvia: Donacidae) and the problem of its sporadic detection in Bivalvia. Evol Int J Org Evol 62: 959-970.
59. Doucet-Beaupré H, Breton S, Chapman EG, Blier PU, Bogan AE, et al. (2010) Mitochondrial phylogenomics of the Bivalvia (Mollusca): Searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol Biol 10: 50.
60. Cao L, Kenchington E, Zouros E, (2004) Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166: 883-894.
61. Cogswell AT, Kenchington ELR, Zouros E, (2006) Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 49: 799-807.
62. Milani L, Ghiselli F, Passamonti M. Sex-linked mitochondrial behavior during early embryo development in Ruditapes philippinarum (Bivalvia Veneridae) a species with the Doubly Uniparental Inheritance (DUI) of mitochondria. J Exp Zool Part B in press.
63. Venetis C, Theologidis I, Zouros E, Rodakis GC, (2006) No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc Biol Sci 273: 2483-2489.
64. Ghiselli F, Milani L, Passamonti M, (2011) Strict sex-specific mtDNA segregation in the germline of the DUI species Venerupis philippinarum (Bivalvia Veneridae). Mol Biol Evol 28: 949-961.
65. Saavedra C, Reyero MI, Zouros E, (1997) Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 145: 1073-1082.
66. Sutherland B, Stewart DT, Kenchington E, Zouros E, (1998) The fate of paternal mitochondrial DNA in developing female mussels, Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genetics 148: 341-347.
67. Kenchington E, MacDonald B, Cao L, Tsagkarakis D, Zouros E, (2002) Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 161: 1579-1588.
68. Ghiselli F, Milani L, Chang PL, Hedgecock D, Davis JP, Nuzhdin SV, Passamonti M, (2011) De Novo Assembly of the Manila clam Ruditapes philippinarum Transcriptome Provides New Insights into Expression Bias, Mitochondrial Doubly Uniparental Inheritance and Sex Determination. Mol Biol Evol doi:10.1093/molbev/msr248.
69. Devauchelle N, (1990) Sexual development and maturity of Tapes philippinarum. In: Tapes philippinarum, biologia e sperimentazione. Ente Sviluppo Agricolo Veneto (ESAV), chapter 3.
70. Hejnol A, (2010) A Twist in Time-The Evolution of Spiral Cleavage in the Light of Animal Phylogeny. Integr Comp Biol 50: 695-706.
71. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
72. Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T, (2000) Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127: 2741-2750.
73. Maurizii MG, Cavaliere V, Gamberi C, Lasko P, Gargiulo G, et al. (2009) Vasa protein is localized in the germ cells and in the oocyte-associated pyriform follicle cells during early oogenesis in the lizard Podarcis sicula. Dev Genes Evol DOI 10.1007/s00427-009-0295-7.
74. Notredame C, Higgins DG, Heringa J, (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
75. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37 (Database Issue): D211-D215.
76. Notredame C, Abergel C, (2003) Using T-Coffee to assess the reliability of multiple sequence alignments. In: Andrade MA, editors. Bioinformatics and Genomes Wymondham, UK Horizon Scientific Press pp. 27-49.
77. Davison A, (2006) The ovotestis: an underdeveloped organ of evolution. BioEssays 28: 642-650.
78. Breton S, Stewart DT, Shepardson S, Trdan RJ, Bogan AE, et al. (2011) Novel Protein Genes in Animal mtDNA: A New Sex Determination System in Freshwater Mussels (Bivalvia: Unionoida)? Mol Biol Evol 28: 1645-1659.
79. Söderström KO, Parvinen M, (1976) Transport of material between the nucleus, the chromatoid body and the Golgi complex in the early spermatids of the rat. Cell Tissue Res 168: 335-342.
80. Peruquetti RL, Taboga SR, de Souza Santos LR, de Oliveira C, de Azeredo-Oliveira MTV, (2011) Nucleolar cycle and chromatoid body formation: Is there a relationship between these two processes during spermatogenesis of Dendropsophus minutus (Amphibia, Anura)? Micron 42: 87-96.
81. Komiya T, Itoh K, Ikenishi K, Furusawa M, (1994) Isolation and characterization of a novel gene of the DEAD Box protein family which is specifically expressed in germ cell of Xenopus laevis. Dev Biol 162: 354-363.
82. Nakao H, (1999) Isolation and characterization of a Bombyx vasa-like gene. Dev Genes Evol 209: 316-321.
83. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP, (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A 97: 9585-9590.
84. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y, (2000) Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 99: 139-142.
85. Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T, (2001) Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev Genes Evol 211: 299-308.
86. Fabioux C, Pouvreau S, Le Roux F, Huvet A, (2004) The oyster vasa-like gene: a specific marker of the germline in Crassostrea gigas. Biochem Bioph Res Co 315: 897-904.
87. Fabioux C, Huvet A, Lelong C, Robert R, Pouvreau S, et al. (2004) Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem Bioph Res Co 320: 592-598.
88. Kakoi S, Kin K, Miyazaki K, Wada H, (2008) Early Development of the Japanese Spiny Oyster (Saccostrea kegaki): Characterization of Some Genetic Markers. Zool Sci 25: 455-464.
89. Swartz SZ, Chan XY, Lambert JD, (2008) Localization of Vasa mRNA during early cleavage of the snail Ilyanassa. Dev Genes Evol 218: 107-113.
90. Kranz AM, Tollenaere A, Norris BJ, Degnan BM, Degnan SM, (2010) Identifying the Germline in an Equally Cleaving Mollusc: Vasa and Nanos Expression During Embryonic and Larval Development of the Vetigastropod Haliotis asinina. J Exp Zool Part B 314: 1-13.
91. Obata M, Sano N, Kimata S, Nagasawa K, Yoshizaki G, Komaru A, (2010) The proliferation and migration of immature germ cells in the mussel, Mytilus galloprovincialis: observation of the expression pattern in the M. galloprovincialis vasa-like gene (Myvlg) by in situ hybridization. Dev Genes Evol 220: 139-149.
92. Extavour CG, Akam M, (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130: 5869-5884.
93. Woods FH, (1931) History of the germ cells in Sphaerium striatinum (Lam.). J Morphol 51: 545-595.
94. Paweletz N, (2001) Walther Flemming: pioneer of mitosis research. Nature Rev Mol Cell Biol 2: 72-75.
95. Skop AR, Liu H, Yates J III, Meyer BJ, Heald R, (2004) Dissection of the Mammalian Midbody Proteome Reveals Conserved Cytokinesis Mechanisms. Science 305: 61-66.
96. Eggert US, Mitchison TJ, Field CM, (2006) Animal Cytokinesis: From Parts List to Mechanisms. Annu Rev Biochem 75: 543-66.
97. Cai S, Weaver LN, Ems-McClung SC, Walczak CE, (2010) Proper Organization of Microtubule Minus Ends Is Needed for Midzone Stability and Cytokinesis. Curr Biol 20: 880-885.
98. Lerit DA, Gavis ER, (2011) Transport of Germ Plasm on Astral Microtubules Directs Germ Cell Development in Drosophila. Curr Biol 21: 439-448.
99. Gönczy P, Echeverri G, Oegema K, Coulson A, Jones SJ, et al. (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408: 331-336.
100. Piano F, Schetter AJ, Mangone M, Stein L, Kemphues KJ, (2000) RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans. Curr Biol 10: 1619-1622.
101. Maeda I, Kohara Y, Yamamoto M, Sugimoto A, (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11: 171-176.
102. Kloc M, Larabell C, Chan AP, Etkin LD, (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75: 81-93.
103. Tyler SEB, Kimber SJ, (2006) The dynamic nature of mollusc egg surface architecture and its relation to the microtubule network. Int J Dev Biol 50: 405-412.
104. Glotzer M, (2009) The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Bio 10: 9-20.
105. Bieliavsky N, Geuskens M, (1990) Interblastomeric plasma membrane formation during cleavage of Xenopus laevis embryos. J Submicrosc Cytol Pathol 22: 445-57.
106. Sutovsky P, Navara CS, Schatten G, (1996) Fate of the Sperm Mitochondria, and the Incorporation, Conversion, and Disassembly of the Sperm Tail Structures during Bovine Fertilization. Biol Reprod 55: 1195-1205.
107. Boldogh IR, Pon LA, (2006) Interactions of mitochondria with the actin cytoskeleton. Biochimica et Biophysica Acta 1763: 450-462.
108. Kogo N, Tazaki A, Kashino Y, Morichika K, Orii H, Mochii M, Watanabe K, (2011) Germ-line mitochondria exhibit suppressed respiratory activity to support their accurate transmission to the next generation. Dev Biol 349: 462-469.