Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 36, 2016, Pages E5261-E5270

  Song, Won Hee ^a   Yi, Young Joo ^a,d   Sutovsky, Miriam ^a   Meyers, Stuart ^b   Sutovsky, Peter ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Missouri   (United States)

^d Chonbuk National University   (South Korea)

Author keywords

Mitochondria|mtDNA; Ubiquitin|autophagy |mitophagy

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; GAMMA AMINOBUTYRIC ACID RECEPTOR ASSOCIATED PROTEIN; HISTONE DEACETYLASE 6; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; MITOCHONDRIAL PROTEIN; PROTEASOME; SEQUESTOSOME 1; UBIQUITIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; ATP DEPENDENT 26S PROTEASE; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; GABARAP PROTEIN, HUMAN; LEUPEPTIN; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL DNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; AUTOPHAGOSOME; AUTOPHAGY; CONFERENCE PAPER; CONTROLLED STUDY; EMBRYO; FERTILIZATION; IMMUNOLOCALIZATION; IN VITRO FERTILIZATION; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOPHAGY; NONHUMAN; OOCYTE; PHARMACOLOGICAL BLOCKING; PIG; PRIORITY JOURNAL; PRONUCLEUS; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; RHESUS MONKEY; SIGNAL TRANSDUCTION; SPERMATOZOON; ZONA PELLUCIDA; ZYGOTE; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MATERNAL INHERITANCE; METABOLISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; DNA, MITOCHONDRIAL; FERTILIZATION; HUMANS; LEUPEPTINS; MACACA MULATTA; MALE; MATERNAL INHERITANCE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL DEGRADATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SEQUESTOSOME-1 PROTEIN; SPERMATOZOA; SWINE; UBIQUITIN; VALOSIN CONTAINING PROTEIN; ZYGOTE;

EID: 84985916502     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605844113     Document Type: Article

References (38)

1. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77(11):6715-6719.
2. Basse CW (2010) Mitochondrial inheritance in fungi. Curr Opin Microbiol 13(6): 712-719.
3. Sutovsky P, et al. (2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63(2):582-590.
4. Sutovsky P, McCauley TC, Sutovsky M, Day BN (2003) Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol Reprod 68(5):1793-1800.
5. Seglen PO, Gordon PB, Holen I (1990) Non-selective autophagy. Semin Cell Biol 1(6): 441-448.
6. Al Rawi S, et al. (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334(6059):1144-1147.
7. Sato M, Sato K (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334(6059):1141-1144.
8. Zhou Q, Li H, Xue D (2011) Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res 21(12):1662-1669.
9. Politi Y, et al. (2014) Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila. Dev Cell 29(3):305-320.
10. Luo SG, et al. (2013) Unique insights into maternal mitochondrial inheritance in mice. Proc Natl Acad Sci USA 110(16):6334-6339.
11. Kraft C, Peter M, Hofmann K (2010) Selective autophagy: Ubiquitin-mediated recognition and beyond. Nat Cell Biol 12(9):836-841.
12. Novak I, et al. (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11(1):45-51.
13. Cataldo L, Baig K, Oko R, Mastrangelo MA, Kleene KC (1996) Developmental expression, intracellular localization, and selenium content of the cysteine-rich protein associated with the mitochondrial capsules of mouse sperm. Mol Reprod Dev 45(3): 320-331.
14. Thompson WE, Ramalho-Santos J, Sutovsky P (2003) Ubiquitination of prohibitin in mammalian sperm mitochondria: Possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 69(1):254-260.
15. Antelman J, et al. (2008) Expression of mitochondrial transcription factor A (TFAM) during porcine gametogenesis and preimplantation embryo development. J Cell Physiol 217(2):529-543.
16. Ashrafi G, Schwarz TL (2013) The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ 20(1):31-42.
17. Sutovsky P, et al. (1999) Ubiquitin tag for sperm mitochondria. Nature 402(6760): 371-372.
18. 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(6):1195-1205.
19. Sutovsky P, Van Leyen K, McCauley T, Day BN, Sutovsky M (2004) Degradation of paternal mitochondria after fertilization: Implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod Biomed Online 8(1):24-33.
20. Kaneda H, et al. (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92(10):4542-4546.
21. Shitara H, et al. (2000) Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 156(3):1277-1284.
22. Vadlamudi RK, Joung I, Strominger JL, Shin J (1996) p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins. J Biol Chem 271(34):20235-20237.
23. Gannavaram S, Sharma P, Duncan RC, Salotra P, Nakhasi HL (2011) Mitochondrial associated ubiquitin fold modifier-1 mediated protein conjugation in Leishmania donovani. PLoS One 6(1):e16156.
24. Ibdah JA, et al. (2001) Lack of mitochondrial trifunctional protein in mice causes neonatal hypoglycemia and sudden death. J Clin Invest 107(11):1403-1409.
25. Jackson S, et al. (1992) Combined enzyme defect of mitochondrial fatty acid oxidation. J Clin Invest 90(4):1219-1225.
26. Cantu D, Schaack J, Patel M (2009) Oxidative inactivation of mitochondrial aconitase results in iron and H2O2-mediated neurotoxicity in rat primary mesencephalic cultures. PLoS One 4(9):e7095.
27. Geyik E, et al. (2014) Investigation of the association between ATP2B4 and ATP5B genes with colorectal cancer. Gene 540(2):178-182.
28. Pankiv S, et al. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282(33):24131-24145.
29. Bjørkøy G, et al. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171(4): 603-614.
30. Komatsu M, Ichimura Y (2010) Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 584(7):1374-1378.
31. Weidberg H, et al. (2010) LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 29(11):1792-1802.
32. Nakamura S, et al. (2001) Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a Piezo-driven pipette: A novel assay for human sperm centrosomal function. Biol Reprod 65(5): 1359-1363.
33. Terada Y, Simerly CR, Hewitson L, Schatten G (2000) Sperm aster formation and pronuclear decondensation during rabbit fertilization and development of a functional assay for human sperm. Biol Reprod 62(3):557-563.
34. Seibenhener ML, et al. (2004) Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 24(18):8055-8068.
35. Xu S, Peng G, Wang Y, Fang S, Karbowski M (2011) The AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover. Mol Biol Cell 22(3):291-300.
36. Tanaka A, et al. (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 191(7):1367-1380.
37. Ju JS, et al. (2009) Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J Cell Biol 187(6):875-888.
38. Kimura S, Noda T, Yoshimori T (2008) Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 33(1):109-122.