DNA packaging proteins Glom and Glom2 coordinately organize the mitochondrial nucleoid of Physarum polycephalum

Mitochondrion

Volumn 11, Issue 4, 2011, Pages 575-586

  Itoh, Kie ^a,b,c   Izumi, Akiko ^c   Mori, Toshiyuki ^d   Dohmae, Naoshi ^d   Yui, Ryoko ^a   Maeda Sano, Katsura ^c,e   Shirai, Yuki ^c   Kanaoka, Masahiro M ^a   Kuroiwa, Tsuneyoshi ^f   Higashiyama, Tetsuya ^a   Sugita, Mamoru ^a   Murakami Murofushi, Kimiko ^c   Kawano, Shigeyuki ^b   Sasaki, Narie ^a,c  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c OCHANOMIZU UNIVERSITY   (Japan)

^d RIKEN   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f RIKKYO UNIVERSITY   (Japan)

Author keywords

DNA packaging protein; Mitochondrial nucleoid; Physarum polycephalum

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL DNA; PROTEIN GLOM; PROTEIN GLOM2; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA PACKAGING; DNA SEQUENCE; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE FUNCTION; HIGH MOBILITY GROUP BOX DOMAIN; HUMAN; IN VITRO STUDY; MITOCHONDRION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSARUM POLYCEPHALUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN RNA BINDING; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; DNA PACKAGING; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; DOWN-REGULATION; FUNGAL PROTEINS; GENES, FUNGAL; HIGH MOBILITY GROUP PROTEINS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYSARUM POLYCEPHALUM; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

PHYSARUM POLYCEPHALUM;

EID: 79957959286     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.03.002     Document Type: Article

References (66)

1. Allan J., Mitchell T., Harborne N., Bohm L., Crane-Robinson C. Roles of H1 domains in determining higher order chromatin structure and H1 location. J. Mol. Biol. 1986, 187:591-601.
2. Antoshechkin I., Bogenhagen D.F. Distinct roles for two purified factors in transcription of Xenopus mitochondrial DNA. Mol. Cell. Biol. 1995, 15:7032-7042.
3. Berger K.H., Yaffe M.P. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol. Cell. Biol. 1998, 18:4043-4052.
4. Bogenhagen D.F., Rousseau D., Burke S. The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 2008, 283:3665-3675.
5. Brewer L.R., Friddle R., Noy A., Baldwin E., Martin S.S., Corzett M., Balhorn R., Baskin R.J. Packaging of single DNA molecules by the yeast mitochondrial protein Abf2p. Biophys. J. 2003, 85:2519-2524.
6. Brown D.T., Izard T., Misteli T. Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat. Struct. Mol. Biol. 2006, 13:250-255.
7. Byrne E.M., Visomirski-Robic L., Cheng Y.W., Rhee A.C., Gott J.M. RNA editing in Physarum mitochondria: assays and biochemical approaches. Meth. Enzymol. 2007, 424:143-172.
8. Chen X.J., Guan M.X., Clark-Walker G.D. MGM101, a nuclear gene involved in maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Nucleic Acids Res. 1993, 21:3473-3477.
9. Chen X.J., Wang X., Kaufman B.A., Butow R.A. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 2005, 307:714-717.
10. Daniel J., Baldwin H. Methods of culture for plasmodia1 myxomycetes. Methods in Cell Physiology 1964, 9-41. Academic Press, New York. D. Prescott (Ed.).
11. Diffley J.F., Stillman B. A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:7864-7868.
12. Diffley J.F., Stillman B. DNA binding properties of an HMG1-related protein from yeast mitochondria. J. Biol. Chem. 1992, 267:3368-3374.
13. Ekstrand M.I., Falkenberg M., Rantanen A., Park C.B., Gaspari M., Hultenby K., Rustin P., Gustafsson C.M., Larsson N.G. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 2004, 13:935-944.
14. Fisher R.P., Clayton D.A. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 1988, 8:3496-3509.
15. Foury F. Cloning and sequencing of the nuclear gene MIP1 encoding the catalytic subunit of the yeast mitochondrial DNA polymerase. J. Biol. Chem. 1989, 264:20552-20560.
16. Foury F., Lahaye A. Cloning and sequencing of the PIF gene involved in repair and recombination of yeast mitochondrial DNA. EMBO J. 1987, 6:1441-1449.
17. Friddle R.W., Klare J.E., Martin S.S., Corzett M., Balhorn R., Baldwin E.P., Baskin R.J., Noy A. Mechanism of DNA compaction by yeast mitochondrial protein Abf2p. Biophys. J. 2004, 86:1632-1639.
18. Ghivizzani S.C., Madsen C.S., Nelen M.R., Ammini C.V., Hauswirth W.W. In organello footprint analysis of human mitochondrial DNA: human mitochondrial transcription factor A interactions at the origin of replication. Mol. Cell. Biol. 1994, 14:7717-7730.
19. Goto A., Matsushima Y., Kadowaki T., Kitagawa Y. Drosophila mitochondrial transcription factor A (d-TFAM) is dispensable for the transcription of mitochondrial DNA in Kc167 cells. Biochem. J. 2001, 354:243-248.
20. Gott J.M., Visomirski L.M., Hunter J.L. Substitutional and insertional RNA editing of the cytochrome c oxidase subunit 1 mRNA of Physarum polycephalum. J. Biol. Chem. 1993, 268:25483-25486.
21. Gott J.M., Parimi N., Bundschuh R. Discovery of new genes and deletion editing in Physarum mitochondria enabled by a novel algorithm for finding edited mRNAs. Nucleic Acids Res. 2005, 33:5063-5072.
22. Greenleaf A.L., Kelly J.L., Lehman I.R. Yeast RPO41 gene product is required for transcription and maintenance of the mitochondrial genome. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:3391-3394.
23. Haindl M., Holler E. Use of the giant multinucleate plasmodium of Physarum polycephalum to study RNA interference in the myxomycete. Anal. Biochem. 2005, 342:194-199.
24. Hines J.C., Ray D.S. The Crithidia fasciculata KAP1 gene encodes a highly basic protein associated with kinetoplast DNA. Mol. Biochem. Parasitol. 1998, 94:41-52.
25. Itoh K., Izumi A., Mori T., Dohmae N., Yui R., Maeda-Sano K., Kanaoka M., Kuroiwa H., Kuroiwa T., Higashiyama T., Murakami-Murofushi K., Kawano S., Sasaki N. New protein Pmn34 with an exonuclease motif localizes in the mitochondrial nucleoid periphery of Physarum polycephalum. Cytologia 2009, 74:401-407.
26. Kanki T., Ohgaki K., Gaspari M., Gustafsson C.M., Fukuoh A., Sasaki N., Hamasaki N., Kang D. Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol. Cell. Biol. 2004, 24:9823-9834.
27. Karkare S., Bhatnagar D. Promising nucleic acid analogs and mimics: characteristic features and applications of PNA, LNA, and morpholino. Appl. Microbiol. Biotechnol. 2006, 71:575-586.
28. Kaufman B.A., Newman S.M., Hallberg R.L., Slaughter C.A., Perlman P.S., Butow R.A. In organello formaldehyde crosslinking of proteins to mtDNA: identification of bifunctional proteins. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7772-7777.
29. Kaufman B.A., Durisic N., Mativetsky J.M., Costantino S., Hancock M.A., Grutter P., Shoubridge E.A. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol. Biol. Cell 2007, 18:3225-3236.
30. Kawano S., Anderson R.W., Nanba T., Kuroiwa T. Polymorphism and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J. Gen. Microbiol. 1987, 133:3175-3182.
31. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 2004, 116:259-272.
32. Kucej M., Butow R.A. Evolutionary tinkering with mitochondrial nucleoids. Trends Cell Biol. 2007, 17:586-592.
33. Kuroiwa T. Studies on mitochondrial structure and function in Physarum polycephalum, III. Electron microscopy of a large amount of DNA releases from a central body in mitochondria by trypsin digestion. J. Cell Biol. 1974, 63:299-306.
34. Kuroiwa T. Mitochondrial nuclei. Int. Rev. Cytol. 1982, 75:1-59.
35. Larsson N.G., Garman J.D., Oldfors A., Barsh G.S., Clayton D.A. A single mouse gene encodes the mitochondrial transcription factor A and a testis-specific nuclear HMG-box protein. Nat. Genet. 1996, 13:296-302.
36. Larsson N.G., Wang J., Wilhelmsson H., Oldfors A., Rustin P., Lewandoski M., Barsh G.S., Clayton D.A. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
37. MacAlpine D.M., Perlman P.S., Butow R.A. The high mobility group protein Abf2p influences the level of yeast mitochondrial DNA recombination intermediates in vivo. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6739-6743.
38. Matsushima Y., Matsumura K., Ishii S., Inagaki H., Suzuki T., Matsuda Y., Beck K., Kitagawa Y. Functional domains of chicken mitochondrial transcription factor A for the maintenance of mitochondrial DNA copy number in lymphoma cell line DT40. J. Biol. Chem. 2003, 278:31149-31158.
39. McCulloch V., Shadel G.S. Human mitochondrial transcription factor B1 interacts with the C-terminal activation region of h-mtTFA and stimulates transcription independently of its RNA methyltransferase activity. Mol. Cell. Biol. 2003, 23:5816-5824.
40. Meeusen S., Nunnari J. Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J. Cell Biol. 2003, 163:503-510.
41. Meeusen S., Tieu Q., Wong E., Weiss E., Schieltz D., Yates J.R., Nunnari J. Mgm101p is a novel component of the mitochondrial nucleoid that binds DNA and is required for the repair of oxidatively damaged mitochondrial DNA. J. Cell Biol. 1999, 145:291-304.
42. Megraw T.L., Chae C.B. Functional complementarity between the HMG1-like yeast mitochondrial histone HM and the bacterial histone-like protein HU. J. Biol. Chem. 1993, 268:12758-12763.
43. Miyakawa I., Fumoto S., Kuroiwa T., Sando N. Characterization of DNA-binding proteins involved in the assembly of mitochondrial nucleoids in the yeast Saccharomyces cerevisiae. Plant Cell Physiol. 1995, 36:1179-1188.
44. Newman S.M., Zelenaya-Troitskaya O., Perlman P.S., Butow R.A. Analysis of mitochondrial DNA nucleoids in wild-type and a mutant strain of Saccharomyces cerevisiae that lacks the mitochondrial HMG box protein Abf2p. Nucleic Acids Res. 1996, 24:386-393.
45. Ohta T., Kawano S., Kuroiwa T. Restriction of amoebo-flagellate (AF) transformation to interphase is related to m phase replication of the centrosome complex in the amoebae of the true slime mould, Physarum polycephalum: a three-dimensional approach. J. Struct. Biol. 1993, 111:105-117.
46. Parisi M.A., Clayton D.A. Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 1991, 252:965-969.
47. Perriere G., Gouy M. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 1996, 78:364-369.
48. Pinchai N., Lee B.S., Holler E. Stage specific expression of poly(malic acid)-affiliated genes in the life cycle of Physarum polycephalum. Spherulin 3b and polymalatase. FEBS J. 2006, 273:1046-1055.
49. Sasaki N., Sakai A., Kawano S., Kuroiwa H., Kuroiwa T. DNA synthesis in isolated mitochondrial nucleoids from plasmodia of Physarum polycephalum. Protoplasma 1998, 203:221-231.
50. Sasaki N., Kuroiwa H., Nishitani C., Takano H., Higashiyama T., Kobayashi T., Shirai Y., Sakai A., Kawano S., Murakami-Murofushi K., Kuroiwa T. Glom is a novel mitochondrial DNA packaging protein in Physarum polycephalum and causes intense chromatin condensation without suppressing DNA functions. Mol. Biol. Cell 2003, 14:4758-4769.
51. Schmid M.B. More than just "histone-like" proteins. Cell 1990, 63:451-453.
52. Spelbrink J.N. Functional organization of mammalian mitochondrial DNA in nucleoids: history, recent developments, and future challenges. IUBMB Life 2010, 62:19-32.
53. Suzuki T., Kawano S., Kuroiwa T. Structure of three-dimensionally rod-shaped mitochondrial nucleoids isolated from the slime mould Physarum polycephalum. J. Cell Sci. 1982, 58:241-261.
54. Takamatsu C., Umeda S., Ohsato T., Ohno T., Abe Y., Fukuoh A., Shinagawa H., Hamasaki N., Kang D. Regulation of mitochondrial D-loops by transcription factor A and single-stranded DNA-binding protein. EMBO Rep. 2002, 3:451-456.
55. Takano H., Abe T., Sakurai R., Moriyama Y., Miyazawa Y., Nozaki H., Kawano S., Sasaki N., Kuroiwa T. The complete DNA sequence of the mitochondrial genome of Physarum polycephalum. Mol. Gen. Genet. 2001, 264:539-545.
56. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 1979, 83:403-427.
57. Van Dyck E., Foury F., Stillman B., Brill S.J. A single-stranded DNA binding protein required for mitochondrial DNA replication in S. cerevisiae is homologous to E. coli SSB. EMBO J. 1992, 11:3421-3430.
58. Wada F., Hasegawa H., Nakamura A., Sugimura Y., Kawai Y., Sasaki N., Shibata H., Maki M., Hitomi K. Identification of substrates for transglutaminase in Physarum polycephalum, an acellular slime mold, upon cellular mechanical damage. FEBS J. 2007, 274:2766-2777.
59. Wang Y., Bogenhagen D.F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J. Biol. Chem. 2006, 281:25791-25802.
60. Wolffe A. Chromatin: Structure and Function 1998, Academic Press, San Diego.
61. Xu C.W., Hines J.C., Engel M.L., Russell D.G., Ray D.S. Nucleus-encoded histone H1-like proteins are associated with kinetoplast DNA in the trypanosomatid Crithidia fasciculata. Mol. Cell. Biol. 1996, 16:564-576.
62. Yoshida Y., Izumi H., Torigoe T., Ishiguchi H., Itoh H., Kang D., Kohno K. P53 physically interacts with mitochondrial transcription factor A and differentially regulates binding to damaged DNA. Cancer Res. 2003, 63:3729-3734.
63. Zelenaya-Troitskaya O., Perlman P.S., Butow R.A. An enzyme in yeast mitochondria that catalyzes a step in branched-chain amino acid biosynthesis also functions in mitochondrial DNA stability. EMBO J. 1995, 14:3268-3276.
64. Zelenaya-Troitskaya O., Newman S.M., Okamoto K., Perlman P.S., Butow R.A. Functions of the high mobility group protein, Abf2p, in mitochondrial DNA segregation, recombination and copy number in Saccharomyces cerevisiae. Genetics 1998, 148:1763-1776.
65. Zlatanova J., Seebart C., Tomschik M. The linker-protein network: control of nucleosomal DNA accessibility. Trends Biochem. Sci. 2008, 33:247-253.
66. Zuo X.M., Clark-Walker G.D., Chen X.J. The mitochondrial nucleoid protein, Mgm101p, of Saccharomyces cerevisiae is involved in the maintenance of rho(+) and ori/rep-devoid petite genomes but is not required for hypersuppressive rho(?) mtDNA. Genetics 2002, 160:1389-1400.