Kinetics and specificity of paternal mitochondrial elimination in Caenorhabditis elegans

Nature Communications

Volumn 7, Issue , 2016, Pages

  Wang, Yang ^a   Zhang, Yi ^a   Chen, Lianwan ^b   Liang, Qian ^a,c   Yin, Xiao Ming ^d   Miao, Long ^b   Kang, Byung Ho ^e   Xue, DIng ^a,f  

^a TSINGHUA UNIVERSITY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c PEKING UNIVERSITY   (China)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^f UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOMYCIN; UNCOUPLING PROTEIN;

ELECTRON MICROSCOPY; HERITABILITY; MITOCHONDRION; NEMATODE; PHYSIOLOGICAL RESPONSE; REACTION KINETICS; TOMOGRAPHY;

ARTICLE; AUTOPHAGY; CAENORHABDITIS ELEGANS; CELL DAMAGE; CELL FUSION; CELL KINETICS; MATERNAL MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; NONHUMAN; PATERNAL MITOCHONDRIA; PATERNAL MITOCHONDRIAL ELIMINATION; ANIMAL; DRUG EFFECT; EMBRYOLOGY; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PHYSIOLOGY;

CAENORHABDITIS ELEGANS; EUKARYOTA;

ANIMALS; AUTOPHAGY; CAENORHABDITIS ELEGANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; OLIGOMYCINS; UNCOUPLING AGENTS;

EID: 84985961725     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12569     Document Type: Article

References (55)

1. Wang, X. The expanding role of mitochondria in apoptosis. Genes Dev. 15, 2922-2933 (2001).
2. Calvo, S. E. & Mootha, V. K. The mitochondrial proteome and human disease. Annu. Rev. Genom. Hum. Genet. 11, 25-44 (2010).
3. Ballard, J. W. & Whitlock, M. C. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729-744 (2004).
4. Wallace, D. C. Mitochondrial DNA mutations in disease and aging. Environ. Mol. Mutagen. 51, 440-450 (2010).
5. Birky, Jr C. W. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl Acad. Sci. USA 92, 11331-11338 (1995).
6. Hutchison, 3rd C. A., Newbold, J. E., Potter, S. S. & Edgell, M. H. Maternal inheritance of mammalian mitochondrial DNA. Nature 251, 536-538 (1974).
7. Wallace, D. C. Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine. Annu. Rev. Biochem. 76, 781-821 (2007).
8. Levine, B. & Elazar, Z. Development. Inheriting maternal mtDNA. Science 334, 1069-1070 (2011).
9. Zhou, Q., Li, H. & Xue, D. Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res. 21, 1662-1669 (2011).
10. Sato, M. & Sato, K. Degradation of paternal mitochondria by fertilizationtriggered autophagy in C. elegans embryos. Science 334, 1141-1144 (2011).
11. Al Rawi, S. et al. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144-1147 (2011).
12. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008).
13. Nakatogawa, H., Suzuki, K., Kamada, Y. & Ohsumi, Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10, 458-467 (2009).
14. Egan, D. F. et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461 (2011).
15. Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434 (2005).
16. Youle, R. J. & van der Bliek, A. M. Mitochondrial fission, fusion, and stress. Science 337, 1062-1065 (2012).
17. Kanki, T. & Klionsky, D. J. Mitophagy in yeast occurs through a selective mechanism. J. Biol. Chem. 283, 32386-32393 (2008).
18. Lemasters, J. J. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuv. Res. 8, 3-5 (2005).
19. Shaw, J. M. & Nunnari, J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178-184 (2002).
20. Chan, D. C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287 (2012).
21. Twig, G. et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446 (2008).
22. Rambold, A. S., Kostelecky, B., Elia, N. & Lippincott-Schwartz, J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl Acad. Sci. USA 108, 10190-10195 (2011).
23. Gomes, L. C., Di Benedetto, G. & Scorrano, L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589-598 (2011).
24. Labrousse, A. M., Zappaterra, M. D., Rube, D. A. & van der Bliek, A. M. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell 4, 815-826 (1999).
25. Breckenridge, D. G., Kang, B. H. & Xue, D. Bcl-2 proteins EGL-1 and CED-9 do not regulate mitochondrial fission or fusion in Caenorhabditis elegans. Curr. Biol. 19, 768-773 (2009).
26. Breckenridge, D. G. et al. Caenorhabditis elegans drp-1 and fis-2 regulate distinct cell-death execution pathways downstream of ced-3 and independent of ced-9. Mol. Cell 31, 586-597 (2008).
27. Kanazawa, T. et al. The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals. PLoS Genet. 4, e1000022 (2008).
28. Jagasia, R., Grote, P., Westermann, B. & Conradt, B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature 433, 754-760 (2005).
29. Santel, A. et al. Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. Cell Sci. 116, 2763-2774 (2003).
30. Otsuga, D. et al. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143, 333-349 (1998).
31. Smirnova, E., Griparic, L., Shurland, D. L. & van der Bliek, A. M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256 (2001).
32. Legros, F., Lombes, A., Frachon, P. & Rojo, M. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 13, 4343-4354 (2002).
33. Eura, Y., Ishihara, N., Yokota, S. & Mihara, K. Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J. Biochem. 134, 333-344 (2003).
34. Susin, S. A. et al. Molecular characterization of mitochondrial apoptosisinducing factor. Nature 397, 441-446 (1999).
35. Wang, X., Yang, C., Chai, J., Shi, Y. & Xue, D. Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298, 1587-1592 (2002).
36. Hecht, R. M., Gossett, L. A. & Jeffery, W. R. Ontogeny of maternal and newly transcribed mRNA analyzed by in situ hybridization during development of Caenorhabditis elegans. Dev. Biol. 83, 374-379 (1981).
37. Scaduto, Jr R. C. & Grotyohann, L. W. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys. J. 76, 469-477 (1999).
38. Melendez, A. et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391 (2003).
39. Tian, Y. et al. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141, 1042-1055 (2010).
40. Zhou, Q. H. et al. Mitochondrial endonuclease G mediates breakdown of paternal mitochondria following fertilization. Science 353, 394-399 (2016).
41. Ashrafi, G. & Schwarz, T. L. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 20, 31-42 (2013).
42. Narendra, D. P. & Youle, R. J. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid. Redox Signal. 14, 1929-1938 (2011).
43. Jia, K. & Levine, B. Autophagy and longevity: lessons from C. elegans. Adv. Exp. Med. Biol. 694, 47-60 (2010).
44. Priault, M. et al. Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ. 12, 1613-1621 (2005).
45. Friedman, J. R. & Nunnari, J. Mitochondrial form and function. Nature 505, 335-343 (2014).
46. Cipolat, S., Martins de Brito, O., Dal Zilio, B. & Scorrano, L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl Acad. Sci. USA 101, 15927-15932 (2004).
47. Griparic, L., van der Wel, N. N., Orozco, I. J., Peters, P. J. & van der Bliek, A. M. Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J. Biol. Chem. 279, 18792-18798 (2004).
48. Olichon, A. et al. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278, 7743-7746 (2003).
49. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
50. Tsang, W. Y. & Lemire, B. D. Stable heteroplasmy but differential inheritance of a large mitochondrial DNA deletion in nematodes. Biochem. Cell Biol. 80, 645-654 (2002).
51. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. & Ahringer, J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002.1-0002.10 (2000).
52. Miller, D. M. & Shakes, D. C. Immunofluorescence microscopy. Methods Cell Biol. 48, 365-394 (1995).
53. Dickinson, D. J., Ward, J. D., Reiner, D. J. & Goldstein, B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10, 1028-1034 (2013).
54. Paix, A. et al. Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 Sites in Caenorhabditis elegans. Genetics 198, 1347-1356 (2014).
55. Toyooka, K. & Kang, B.H. Reconstructing plant cells in 3D by serial section electron tomography. Methods Mol. Biol. 1080, 159-170 (2014).