Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development

Journal of Cell Biology

Volumn 160, Issue 2, 2003, Pages 189-200

  Chen, Hsiuchen ^a   Detmer, Scott A ^a   Ewald, Andrew J ^a   Griffin, Erik E ^a   Fraser, Scott E ^a   Chan, David C ^a,b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b MC114 96 ^*  (United States)

Author keywords

GTPase; Knockout; Membrane fusion; Mice; Mitochondria

Indexed keywords

MITOCHONDRIAL PROTEIN; MITOFUSIN 1; MITOFUSIN 2; UNCLASSIFIED DRUG;

ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; FIBROBLAST; MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TROPHOBLAST;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETAL PROTEINS; EMBRYO; EMBRYO LOSS; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, LETHAL; GTP PHOSPHOHYDROLASES; INTRACELLULAR MEMBRANES; MACROMOLECULAR SUBSTANCES; MALE; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PLACENTA; TROPHOBLASTS; UTROPHIN;

VERTEBRATA;

EID: 0037455575     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200211046     Document Type: Article

References (51)

1. Bakeeva, L.E., S. Chentsov Yu, and V.P. Skulachev. 1978. Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochim. Biophys. Acta. 501:349-369.
2. Bakeeva, L.E., Y.S. Chentsov, and V.P. Skulachev. 1981. Ontogenesis of mitochondrial reticulum in rat diaphragm muscle. Eur. J. Cell Biol. 25:175-181.
3. Bakeeva, L.E., S. Chentsov Yu, and V.P. Skulachev. 1983. Intermitochondrial contacts in myocardiocytes. J. Mol. Cell. Cardiol. 15:413-420.
4. Bereiter-Hahn, J., and M. Voth. 1994. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27:198-219.
5. Bleazard, W., J.M. McCaffery, E.J. King, S. Bale, A. Mozdy, Q. Tieu, J. Nunnari, and J.M. Shaw. 1999. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1:298-304.
6. Bourne, H.R., D.A. Sanders, and F. McCormick. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 349:117-127.
7. Chester, N., F. Kuo, C. Kozak, C.D. O'Hara, and P. Leder. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12:3382-3393.
8. Collins, T.J., M.J. Berridge, P. Lipp, and M.D. Bootman. 2002. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21: 1616-1627.
9. Copp, A.J. 1995. Death before birth: clues from gene knockouts and mutations. Trends Genet. 11:87-93.
10. Cross, J.C. 2000. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin. Cell Dev. Biol. 11: 105-113.
11. Edgar, B.A., and T.L. Orr-Weaver. 2001. Endoreplication cell cycles: more for less. Cell. 105:297-306.
12. Enriquez, J.A., J. Cabezas-Herrera, M.P. Bayona-Bafaluy, and G. Attardi. 2000. Very rare complementation between mitochondria carrying different mitochondrial DNA mutations points to intrinsic genetic autonomy of the organelles in cultured human cell. J. Biol. Chem. 275:11207-11215.
13. Faria, T.N., L. Ogren, F. Talamantes, D.I. Linzer, and M.J. Soares. 1991. Localization of placental lactogen-I in trophoblast giant cells of the mouse placenta. Biol. Reprod. 44:327-331.
14. Fekkes, P., K.A. Shepard, and M.P. Yaffe. 2000. Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J. Cell Biol. 151: 333-340.
15. Frank, S., B. Gaume, E.S. Bergmann-Leitner, W.W. Leitner, E.G. Robert, F. Catez, C.L. Smith, and R.J. Youle. 2001. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:515-525.
16. Hales, K.G., and M.T. Fuller. 1997. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 90:121-129.
17. Hayashi, J., M. Takemitsu, Y. Goto, and I. Nonaka. 1994. Human mitochondria and mitochondrial genome function as a single dynamic cellular unit. J. Cell Biol. 125:43-50.
18. Hermann, G.J., J.W. Thatcher, J.P. Mills, K.G. Hales, M.T. Fuller, J. Nunnari, and J.M. Shaw. 1998. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143:359-373.
19. Hesse, M., T. Franz, Y. Tamai, M.M. Taketo, and T.M. Magin. 2000. Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. EMBO J. 19:5060-5070.
20. Hwa, J.J., M.A. Hiller, M.T. Fuller, and A. Santel. 2002. Differential expression of the Drosophila mitofusin genes fuzzy onions (fzo) and dmfn. Mech. Dev. 116: 213-216.
21. Jacquemin, P., V. Sapin, E. Alsat, D. Evain-Brion, P. Dolle, and I. Davidson. 1998. Differential expression of the TEF family of transcription factors in the murine placenta and during differentiation of primary human trophoblasts in vitro. Dev. Dyn. 212:423-436.
22. Jat, P.S., C.L. Cepko, R.C. Mulligan, and P.A. Sharp. 1986. Recombinant retroviruses encoding simian virus 40 large T antigen and polyomavirus large and middle T antigens. Mol. Cell. Biol. 6:1204-1217.
23. Kraut, N., L. Snider, C.M. Chen, S.J. Tapscott, and M. Groudine. 1998. Requirement of the mouse I-mfa gene for placental development and skeletal patterning. EMBO J. 17:6276-6288.
24. Kunkel, T.A., K. Bebenek, and J. McClary. 1991. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204:125-139.
25. Lee, S.J., F. Talamantes, E. Wilder, D.I. Linzer, and D. Nathans. 1988. Trophoblastic giant cells of the mouse placenta as the site of proliferin synthesis. Endocrinology. 122:1761-1768.
26. Lescisin, K.R., S. Varmuza, and J. Rossant. 1988. Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev. 2:1639-1646.
27. Loew, L.M. 1999. Potentiometric membrane dyes and imaging membrane potential in single cells. In Fluorescent and Luminescent Probes for Biological Activity. W.T. Mason, editor. Academic Press, London. 210-221.
28. Lupas, A. 1996. Coiled coils: new structures and new functions. Trends Biochem. Sci. 21:375-382.
29. Morris, R.L., and P.J. Hollenbeck. 1995. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 131:1315-1326.
30. Mozdy, A.D., J.M. McCaffery, and J.M. Shaw. 2000. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fislp. J. Cell Biol. 151:367-380.
31. Nakada, K., K. Inoue, and J. Hayashi. 2001a. Interaction theory of mammalian mitochondria. Biochem. Biophys. Res. Commun. 288:743-746.
32. Nakada, K., K. Inoue, T. Ono, K. Isobe, A. Ogura, Y.I. Goto, I. Nonaka, and J.I. Hayashi. 2001b. Inter-mitochondrial complementation: Mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat. Med. 7:934-940.
33. Nangaku, M., R. Sato-Yoshitake, Y. Okada, Y. Noda, R. Takemura, H. Yamazaki, and N. Hirokawa. 1994. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell. 79:1209-1220.
34. Nunnari, J., W.F. Marshall, A. Straight, A. Murray, J.W. Sedat, and P. Walter. 1997. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8:1233-1242.
35. Okada, A., R. Lansford, J.M. Weimann, S.E. Fraser, and S.K. McConnell. 1999. Imaging cells in the developing nervous system with retrovirus expressing modified green fluorescent protein. Exp. Neurol. 156:394-406.
36. Ono, T., K. Isobe, K. Nakada, and J.I. Hayashi. 2001. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat. Genet. 28:272-275.
37. Rapaport, D., M. Brunner, W. Neupert, and B. Westermann. 1998. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J. Biol. Chem. 273:20150-20155.
38. Riley, P., L. Anson-Cartwright, and J.C. Cross. 1998. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat. Genet. 18:271-275.
39. Rizzuto, R., P. Pinton, W. Carrington, F.S. Fay, K.E. Fogarty, L.M. Lifshitz, R.A. Tuft, and T. Pozzan. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 280:1763-1766.
40. Rojo, M., F. Legros, D. Chateau, and A. Lombes. 2002. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115:1663-1674.
41. Santel, A., and M.T. Fuller. 2001. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114:867-874.
42. Scott, I.C., L. Anson-Cartwright, P. Riley, D. Reda, and J.C. Cross. 2000. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol. Cell. Biol. 20:530-541.
43. Sesaki, H., and R.E. Jensen. 1999. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147:699-706.
44. Smirnova, E., L. Griparic, D.L. Shurland, and A.M. van Der Bliek. 2001. Dynamin-related protein drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell. 12:2245-2256.
45. Sprang, S.R. 1997. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66:639-678.
46. Talosi, G., E. Endreffy, S. Turi, and I. Nemeth. 2000. Molecular and genetic aspects of preeclampsia: state of the art. Mol. Genet. Metab. 71:565-572.
47. Tanaka, S., T. Kunath, A.K. Hadjantonakis, A. Nagy, and J. Rossant. 1998a. Promotion of trophoblast stem cell proliferation by FGF4. Science. 282:2072-2075.
48. Tanaka, Y., Y. Kanai, Y. Okada, S. Nonaka, S. Takeda, A. Harada, and N. Hirokawa. 1998b. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell. 93:1147-1158.
49. Tieu, Q., and J. Nunnari. 2000. Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell Biol. 151:353-366.
50. Vortkamp, A., K. Lee, B. Lanske, G.V. Segre, H.M. Kronenberg, and C.J. Tabin. 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 273:613-622.
51. Widschwendter, M., H. Schrocksnadel, and M.G. Mortl. 1998. Pre-eclampsia: a disorder of placental mitochondria? Mol. Med. Today. 4:286-291.