Abstract
The nematode C. elegans represents a powerful experimental system with key properties and advantages to study the mechanisms underlying mitochondrial DNA maternal inheritance and paternal components sorting. First, the transmission is uniparental and maternal as in many animal species; second, at fertilization sperm cells contain both mitochondria and mtDNA; and third, the worm allows powerful genetics and cell biology approaches to characterize the mechanisms underlying the uniparental and maternal transmission of mtDNA. Fertilization of C. elegans oocyte occurs inside the transparent body when the mature oocyte resumes meiosis I and passes through the spermatheca. One amoeboid sperm cell fuses with the oocyte and delivers its whole content. Among the structures entering the embryo, the sperm mitochondria and a fraction of the nematode-specific membranous organelles are rapidly degraded, whereas others like centrioles and sperm genomic DNA are transmitted. In this chapter, we will review the knowledge acquired on sperm inherited organelles clearance during the recent years using C. elegans.
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Al Rawi S, Louvet-Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334:1144–1147
Alberti A, Michelet X, Djeddi A, Legouis R (2010) The autophagosomal protein LGG-2 acts synergistically with LGG-1 in dauer formation and longevity in C. elegans. Autophagy 6:622–633
Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465
Chatterjee I, Richmond A, Putiri E, Shakes DC, Singson A (2005) The Caenorhabditis elegans spe-38 gene encodes a novel four-pass integral membrane protein required for sperm function at fertilization. Development 132:2795–2808
Djeddi A, Al Rawi S, Deuve JL, Perrois C, Liu YY, Russeau M, Sachse M, Galy V (2015) Sperm-inherited organelle clearance in C. elegans relies on LC3-dependent autophagosome targeting to the pericentrosomal area. Development 142:1705–1716
Eura Y, Ishihara N, Yokota S, Mihara K (2003) Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J Biochem 134:333–344
Fawcett DW (1981) The cell. W. B. Saunders, Philadelphia
Hajjar C, Sampuda KM, Boyd L (2014) Dual roles for ubiquitination in the processing of sperm organelles after fertilization. BMC Dev Biol 14:6
Italiano JE Jr, Roberts TM, Stewart M, Fontana CA (1996) Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell 84:105–114
Jacob WA, Bakker A, Hertsens RC, Biermans W (1994) Mitochondrial matrix granules: their behavior during changing metabolic situations and their relationship to contact sites between inner and outer mitochondrial membranes. Microsc Res Tech 27:307–318
Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4(5):815–826
Lambert CC, Epel D (1979) Calcium-mediated mitochondrial movement in ascidian sperm during fertilization. Dev Biol 69:296–304
Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9:99–111
Liau WS, Gonzalez-Serricchio AS, Deshommes C, Chin K, Lamunyon CW (2007) A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genet 8:8
Luo SM, Ge ZJ, Wang ZW, Jiang ZZ, Wang ZB, Ouyang YC, Hou Y, Schatten H, Sun QY (2013) Unique insights into maternal mitochondrial inheritance in mice. Proc Natl Acad Sci U S A 110:13038–13043
Machaca K, L’Hernault SW (1997) The Caenorhabditis elegans spe-5 gene is required for morphogenesis of a sperm-specific organelle and is associated with an inherent cold-sensitive phenotype. Genetics 146:567–581
Manil-Segalen M, Lefebvre C, Jenzer C, Trichet M, Boulogne C, Satiat-Jeunemaitre B, Legouis R (2014) The C. elegans LC3 acts downstream of GABARAP to degrade autophagosomes by interacting with the HOPS subunit VPS39. Dev Cell 28:43–55
Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301:1387–1391
Nelson GA, Ward S (1980) Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19:457–464
Nishimura H, L’Hernault SW (2017) Spermatogenesis. Curr Biol 27:R988–R994
Nishimura Y, Yoshinari T, Naruse K, Yamada T, Sumi K, Mitani H, Higashiyama T, Kuroiwa T (2006) Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci U S A 103:1382–1387
Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498
Palmisano NJ, Melendez A (2018) Autophagy in C. elegans development. Dev Biol. https://doi.org/10.1016/j.ydbio.2018.04.009
Politi Y, Gal L, Kalifa Y, Ravid L, Elazar Z, Arama E (2014) Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila. Dev Cell 29:305–320
Roberts TM, Pavalko FM, Ward S (1986) Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J Cell Biol 102:1787–1796
Rojansky R, Cha MY, Chan DC (2016) Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. elife 5:e17896. https://doi.org/10.7554/eLife.17896
Rolland SG, Lu Y, David CN, Conradt B (2009) The BCL-2-like protein CED-9 of C. elegans promotes FZO-1/Mfn1,2- and EAT-3/Opa1-dependent mitochondrial fusion. J Cell Biol 186:525–540
Sato M, Sato K (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334:1141–1144
Sato M, Sato K, Tomura K, Kosako H, Sato K (2018) The autophagy receptor ALLO-1 and the IKKE-1 kinase control clearance of paternal mitochondria in Caenorhabditis elegans. Nat Cell Biol 20:81–91
Shakes DC, Ward S (1989) Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 134:307–316
Sharpley MS, Marciniak C, Eckel-Mahan K, McManus M, Crimi M, Waymire K, Lin CS, Masubuchi S, Friend N, Koike M, Chalkia D, Macgregor G, Sassone-Corsi P, Wallace DC (2012) Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell 151:333–343
Smith JR, Stanfield GM (2011) TRY-5 is a sperm-activating protease in Caenorhabditis elegans seminal fluid. PLoS Genet 7:e1002375
Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (1999) Ubiquitin tag for sperm mitochondria. Nature 402:371–372
Tsang WY, Lemire BD (2002a) Mitochondrial genome content is regulated during nematode development. Biochem Biophys Res Commun 291:8–16
Tsang WY, Lemire BD (2002b) Stable heteroplasmy but differential inheritance of a large mitochondrial DNA deletion in nematodes. Biochem Cell Biol 80:645–654
Tsang WY, Lemire BD (2003) The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim Biophys Acta 1638:91–105
Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N (2008) Autophagy is essential for preimplantation development of mouse embryos. Science 321:117–120
van der Bliek AM, Shen Q, Kawajiri S (2013) Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol 5:a011072. https://doi.org/10.1101/cshperspect.a011072
Wang Y, Zhang Y, Chen L, Liang Q, Yin XM, Miao L, Kang BH, Xue D (2016) Kinetics and specificity of paternal mitochondrial elimination in Caenorhabditis elegans. Nat Commun 7:12569
Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304–321
Ward S, Argon Y, Nelson GA (1981) Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91:26–44
Washington NL, Ward S (2006) FER-1 regulates Ca2+-mediated membrane fusion during C. elegans spermatogenesis. J Cell Sci 119:2552–2562
Wei Y, Chiang WC, Sumpter R Jr, Mishra P, Levine B (2017) Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell 168:224–238.e10
Wolf N, Hirsh D, Mcintosh JR (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63:155–169
Xu XZ, Sternberg PW (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285–297
Zamponi N, Zamponi E, Cannas SA, Billoni OV, Helguera PR, Chialvo DR (2018) Mitochondrial network complexity emerges from fission/fusion dynamics. Sci Rep 8:363
Zhang Y, Yan L, Zhou Z, Yang P, Tian E, Zhang K, Zhao Y, Li Z, Song B, Han J, Miao L, Zhang H (2009) SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell 136:308–321
Zhou Q, Li H, Xue D (2011) Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res 21:1662–1669
Zhou Q, Li H, Li H, Nakagawa A, Lin JL, Lee ES, Harry BL, Skeen-Gaar RR, Suehiro Y, William D, Mitani S, Yuan HS, Kang BH, Xue D (2016) Mitochondrial endonuclease G mediates breakdown of paternal mitochondria upon fertilization. Science 353:394–399
Acknowledgments
Our laboratory is supported by the Fondation pour la Recherche Medicale (Equipe FRM DEQ20160334874) and the European COST Program (BM1408 GENiE). We are grateful to Martin Sachse from Institut Pasteur Paris for the TEM and Charlène Perrois, Valeria Parrales, and Sebastien Normant for their technical support.
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Merlet, J., Rubio-Peña, K., Al Rawi, S., Galy, V. (2019). Autophagosomal Sperm Organelle Clearance and mtDNA Inheritance in C. elegans . In: Sutovsky, P. (eds) Cellular and Molecular Basis of Mitochondrial Inheritance. Advances in Anatomy, Embryology and Cell Biology, vol 231. Springer, Cham. https://doi.org/10.1007/102_2018_1
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DOI: https://doi.org/10.1007/102_2018_1
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