Evolution of centrosomes and the nuclear lamina: Amoebozoan assets

European Journal of Cell Biology

Volumn 94, Issue 6, 2015, Pages 249-256

  Gräf, Ralph ^a   Batsios, Petros ^a   Meyer, Irene ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Basal body; Centriole; Centrosome; Lamin; LEM domain; LINC complex; Nuclear envelope; Nuclear lamina; Sun1

Indexed keywords

ENVELOPE PROTEIN; LAMIN; CHROMATIN;

ALVEOLATA; AMOEBOZOA; ARCHAEPLASTIDA; CELL NUCLEUS MEMBRANE; CELL ORGANELLE; CENTRIOLE; CENTROSOME; CHROMATIN; DICTYOSTELIUM DISCOIDEUM; EXCAVATA; KINETOSOME; LAST COMMON ANCESTOR; MICROTUBULE ORGANIZING CENTER; MITOCHONDRION; NONHUMAN; NUCLEAR LAMINA; OPISTHOKONTA; PRIORITY JOURNAL; RHIZARIA; SHORT SURVEY; STRAMENOPILE; AMOEBA (LIFE CYCLE STAGE); ANIMAL; DICTYOSTELIUM; EVOLUTION; HUMAN; METABOLISM; PHYLOGENY;

ALVEOLATA; AMOEBOZOA; ARCHAEPLASTIDA; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; EXCAVATA; FUNGI/METAZOA GROUP; RHIZARIA;

AMOEBA; ANIMALS; BIOLOGICAL EVOLUTION; CENTROSOME; CHROMATIN; DICTYOSTELIUM; HUMANS; NUCLEAR LAMINA; PHYLOGENY;

EID: 84983177642     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2015.04.004     Document Type: Short Survey

References (89)

1. Adl S.M., Simpson A.G., Lane C.E., Lukes J., Bass D., Bowser S.S., Brown M.W., Burki F., Dunthorn M., Hampl V., Heiss A., Hoppenrath M., Lara E., Le Gall L., Lynn D.H., McManus H., Mitchell E.A., Mozley-Stanridge S.E., Parfrey L.W., Pawlowski J., Rueckert S., Shadwick R.S., Schoch C.L., Smirnov A., Spiegel F.W. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012, 59:429-493.
2. Akiyoshi B., Gull K. Evolutionary cell biology of chromosome segregation: insights from trypanosomes. Open Biol. 2013, 3:130023.
3. Al Jord A., Lemaitre A.I., Delgehyr N., Faucourt M., Spassky N., Meunier A. Centriole amplification by mother and daughter centrioles differs in multiciliated cells. Nature 2014, 516:104-107.
4. Al-Bassam J., Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 2011, 21:604-614.
5. Al-Haboubi T., Shumaker D.K., Koser J., Wehnert M., Fahrenkrog B. Distinct association of the nuclear pore protein Nup153 with A- and B-type lamins. Nucleus 2011, 2:500-509.
6. Araki M., Masutani C., Takemura M., Uchida A., Sugasawa K., Kondoh J., Ohkuma Y., Hanaoka F. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 2001, 276:18665-18672.
7. Azimzadeh J. Exploring the evolutionary history of centrosomes. Philos. Trans. R. Soc. London, Ser. B: Biol. Sci. 2014, 369. 10.1098/rstb.2013.0453.
8. Azimzadeh J., Wong M.L., Downhour D.M., Sanchez Alvarado A., Marshall W.F. Centrosome loss in the evolution of planarians. Science 2012, 335:461-463.
9. Basto R., Lau J., Vinogradova T., Gardiol A., Woods C.G., Khodjakov A., Raff J.W. Flies without centrioles. Cell 2006, 125:1375-1386.
10. Batsios P., Peter T., Baumann O., Stick R., Meyer I., Gräf R. A lamin in lower eukaryotes?. Nucleus 2012, 3:237-243.
11. Benchimol M. The nuclei of Giardia lamblia-new ultrastructural observations. Arch. Microbiol. 2005, 183:160-168.
12. Bobinnec Y., Khodjakov A., Mir L.M., Rieder C.L., Edde B., Bornens M. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 1998, 143:1575-1589.
13. Bornens M., Azimzadeh J. Origin and evolution of the centrosome. Adv. Exp. Med. Biol. 2007, 607:119-129.
14. Brachner A., Foisner R. Evolvement of LEM proteins as chromatin tethers at the nuclear periphery. Biochem. Soc. Trans. 2011, 39:1735-1741.
15. Caetano-Anolles G., Nasir A., Zhou K., Caetano-Anolles D., Mittenthal J.E., Sun F.J., Kim K.M. Archaea: the first domain of diversified life. Archaea 2014, 2014:590214.
16. Caputo S., Couprie J., Duband-Goulet I., Konde E., Lin F., Braud S., Gondry M., Gilquin B., Worman H.J., Zinn-Justin S. The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. J. Biol. Chem. 2006, 281:18208-18215.
17. Cardona A., Hartenstein V., Romero R. Early embryogenesis of planaria: a cryptic larva feeding on maternal resources. Dev. Genes Evol. 2006, 216:667-681.
18. Carvalho-Santos Z., Azimzadeh J., Pereira-Leal J.B., Bettencourt-Dias M. Evolution: tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 2011, 194:165-175.
19. Carvalho-Santos Z., Machado P., Branco P., Tavares-Cadete F., Rodrigues-Martins A., Pereira-Leal J.B., Bettencourt-Dias M. Stepwise evolution of the centriole-assembly pathway. J. Cell Sci. 2010, 123:1414-1426.
20. Cavalier-Smith T. Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol. Dir. 2010, 5:7.
21. Chapman M.J., Dolan M.F., Margulis L. Centrioles and kinetosomes: form, function, and evolution. Q. Rev. Biol. 2000, 75:409-429.
22. Ciska M., Masuda K., Moreno Diaz de la Espina S. Lamin-like analogues in plants: the characterization of NMCP1 in Allium cepa. J. Exp. Bot. 2013, 64:1553-1564.
23. Crisp M., Liu Q., Roux K., Rattner J.B., Shanahan C., Burke B., Stahl P.D., Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 2006, 172:41-53.
24. Dahl K.N., Kahn S.M., Wilson K.L., Discher D.E. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 2004, 117:4779-4786.
25. Dantas T.J., Daly O.M., Morrison C.G. Such small hands: the roles of centrins/caltractins in the centriole and in genome maintenance. Cell. Mol. Life Sci. 2012, 69:2979-2997.
26. Daunderer C., Schliwa M., Gräf R. Dictyostelium centrin-related protein (DdCrp), the most divergent member of the centrin family, possesses only two EF hands and dissociates from the centrosome during mitosis. Eur. J. Cell Biol. 2001, 80:621-630.
27. De Souza C.P., Osmani S.A. Mitosis, not just open or closed. Eukaryot. Cell 2007, 6:1521-1527.
28. Debec A., Sullivan W., Bettencourt-Dias M. Centrioles: active players or passengers during mitosis?. Cell. Mol. Life Sci. 2010, 67:2173-2194.
29. Devos D.P., Gräf R., Field M.C. Evolution of the nucleus. Curr. Opin. Cell Biol. 2014, 28C:8-15.
30. Ding R., West R.R., Morphew M., Oakley B.R., McIntosh J.R. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol. Biol. Cell 1997, 8:1461-1479.
31. DuBois K.N., Alsford S., Holden J.M., Buisson J., Swiderski M., Bart J.M., Ratushny A.V., Wan Y., Bastin P., Barry J.D., Navarro M., Horn D., Aitchison J.D., Rout M.P., Field M.C. NUP-1 is a large coiled-coil nucleoskeletal protein in trypanosomes with lamin-like functions. PLoS Biol. 2012, 10:e1001287.
32. Ehler L.L., Holmes J.A., Dutcher S.K. Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. Genetics 1995, 141:945-960.
33. Fededa J.P., Gerlich D.W. Molecular control of animal cell cytokinesis. Nat. Cell Biol. 2012, 14:440-447.
34. Fedorchak G.R., Kaminski A., Lammerding J. Cellular mechanosensing: getting to the nucleus of it all. Prog. Biophys. Mol. Biol. 2014, 111:76-92.
35. Field M.C., Horn D., Alsford S., Koreny L., Rout M.P. Telomeres, tethers and trypanosomes. Nucleus 2012, 3:478-486.
36. Fong K.W., Choi Y.K., Rattner J.B., Qi R.Z. CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the {gamma}-tubulin ring complex. Mol. Biol. Cell 2008, 19:115-125.
37. Friedländer M., Wahrman J. The spindle as a basal body distributor. A study in the meiosis of the male silkworm moth, Bombyx mori. J. Cell Sci. 1970, 7:65-89.
38. Giansanti M.G., Bucciarelli E., Bonaccorsi S., Gatti M. Drosophila SPD-2 is an essential centriole component required for pcm recruitment and astral-microtubule nucleation. Curr. Biol. 2008, 18:303-309.
39. Glöckner G., Golderer G., Werner-Felmayer G., Meyer S., Marwan W. A first glimpse at the transcriptome of Physarum polycephalum. BMC Genomics 2008, 9:6.
40. Gräf R. Microtubule Organization in Dictyostelium, Encyclopedia of Life Sciences (ELS) 2015, John Wiley & Sons, Ltd, Chichester. 10.1002/9780470015902.a9780470021852.pub9780470015902.
41. Graumann K. Evidence for LINC1-SUN associations at the plant nuclear periphery. PLoS ONE 2014, 9:e93406.
42. Haque F., Lloyd D.J., Smallwood D.T., Dent C.L., Shanahan C.M., Fry A.M., Trembath R.C., Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol. Cell Biol. 2006, 26:3738-3751.
43. Hartman H., Fedorov A. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1420-1425.
44. Herrmann H., Bar H., Kreplak L., Strelkov S.V., Aebi U. Intermediate filaments: from cell architecture to nanomechanics. Nat. Rev. Mol. Cell Biol. 2007, 8:562-573.
45. Hodges M.E., Scheumann N., Wickstead B., Langdale J.A., Gull K. Reconstructing the evolutionary history of the centriole from protein components. J. Cell Sci. 2010, 123:1407-1413.
46. Kaller M., Euteneuer U., Nellen W. Differential effects of heterochromatin protein 1 isoforms on mitotic chromosome distribution and growth in Dictyostelium discoideum. Eukaryot. Cell 2006, 5:530-543.
47. Keller L.C., Wemmer K.A., Marshall W.F. Influence of centriole number on mitotic spindle length and symmetry. Cytoskeleton (Hoboken) 2010, 67:504-518.
48. Khodjakov A., Cole R.W., Oakley B.R., Rieder C.L. Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 2000, 10:59-67.
49. Khodjakov A., Rieder C.L. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 2001, 153:237-242.
50. King M.C., Drivas T.G., Blobel G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 2008, 134:427-438.
51. Koblenz B., Schoppmeier J., Grunow A., Lechtreck K.F. Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. J. Cell Sci. 2003, 116:2635-2646.
52. Krüger A., Batsios P., Baumann O., Luckert E., Schwarz H., Stick R., Meyer I., Gräf R. Characterization of NE81, the first lamin-like nucleoskeleton protein in a unicellular organism. Mol. Biol. Cell 2012, 23:360-370.
53. Kuhnert O., Baumann O., Meyer I., Gräf R. Functional characterization of CP148, a novel key component for centrosome integrity in Dictyostelium. Cell. Mol. Life Sci. 2012, 69:1875-1888.
54. Li S., Sandercock A.M., Conduit P., Robinson C.V., Williams R.L., Kilmartin J.V. Structural role of Sfi1p-centrin filaments in budding yeast spindle pole body duplication. J. Cell Biol. 2006, 173:867-877.
55. Lin T.C., Neuner A., Schlosser Y.T., Scharf A.N., Weber L., Schiebel E. Cell-cycle dependent phosphorylation of yeast pericentrin regulates gamma-TuSC-mediated microtubule nucleation. Elife 2014, 3:e02208.
56. Lucas E.P., Raff J.W. Maintaining the proper connection between the centrioles and the pericentriolar matrix requires Drosophila centrosomin. J. Cell Biol. 2007, 178:725-732.
57. Lynch M., Field M.C., Goodson H.V., Malik H.S., Pereira-Leal J.B., Roos D.S., Turkewitz A.P., Sazer S. Evolutionary cell biology: two origins, one objective. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:16990-16994.
58. Mana-Capelli S., Gräf R., Larochelle D.A. Dictyostelium discoideum CenB is a bona fide centrin essential for nuclear architecture and centrosome stability. Eukaryot. Cell 2009, 8:1106-1117.
59. Megraw T.L., Li K., Kao L.R., Kaufman T.C. The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development 1999, 126:2829-2839.
60. Pace N.R. Time for a change. Nature 2006, 441:289.
61. Pappas G.D. The fine structure of the nuclear envelope of Amoeba proteus. J. Biophys. Biochem. Cytol. 1956, 2:431-434.
62. Pearson C.G., Winey M. Basal body assembly in ciliates: the power of numbers. Traffic 2009, 10:461-471.
63. Pedersen L.B., Schroder J.M., Satir P., Christensen S.T. The ciliary cytoskeleton. Compre. Physiol. 2012, 2:779-803.
64. Pickett-Heaps J.D. The autonomy of the centriole: fact or fallacy?. Cytobios 1971, 3:205-214.
65. Rajgor D., Shanahan C.M. Nesprins: from the nuclear envelope and beyond. Expert Rev. Mol. Med. 2013, 15:e5.
66. Rothballer A., Kutay U. The diverse functional LINCs of the nuclear envelope to the cytoskeleton and chromatin. Chromosoma 2013, 122:415-429.
67. Samejima I., Lourenco P.C., Snaith H.A., Sawin K.E. Fission yeast mto2p regulates microtubule nucleation by the centrosomin-related protein mto1p. Mol. Biol. Cell 2005, 16:3040-3051.
68. Schneider M., Lu W., Neumann S., Brachner A., Gotzmann J., Noegel A.A., Karakesisoglou I. Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell. Mol. Life Sci. 2011, 68:1593-1610.
69. Schulz I., Baumann O., Samereier M., Zoglmeier C., Gräf R. Dictyostelium Sun1 is a dynamic membrane protein of both nuclear membranes and required for centrosomal association with clustered centromeres. Eur. J. Cell Biol. 2009, 88:621-638.
70. Schulz I., Erle A., Gräf R., Kruger A., Lohmeier H., Putzler S., Samereier M., Weidenthaler S. Identification and cell cycle-dependent localization of nine novel, genuine centrosomal components in Dictyostelium discoideum. Cell Motil. Cytoskeleton 2009, 66:915-928.
71. Simpson J.G., Roberts R.G. Patterns of evolutionary conservation in the nesprin genes highlight probable functionally important protein domains and isoforms. Biochem. Soc. Trans. 2008, 36:1359-1367.
72. Solnica-Krezel L., Burland T.G., Dove W.F. Variable pathways for developmental changes of mitosis and cytokinesis in Physarum polycephalum. J. Cell Biol. 1991, 113:591-604.
73. Solnica-Krezel L., Diggins-Gilicinski M., Burland T.G., Dove W.F. Variable pathways for developmental changes in composition and organization of microtubules in Physarum polycephalum. J. Cell Sci. 1990, 96(Pt 3):383-393.
74. Starr D.A., Fridolfsson H.N. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 2010, 26:421-444.
75. Stewart-Hutchinson P.J., Hale C.M., Wirtz D., Hodzic D. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell Res. 2008, 314:1892-1905.
76. Still I.H., Vettaikkorumakankauv A.K., DiMatteo A., Liang P. Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms. BMC Evol. Biol. 2004, 4:16.
77. Sukumaran S.K., Blau-Wasser R., Rohlfs M., Gallinger C., Schleicher M., Noegel A.A. The centrosomal component CEP161 of Dictyostelium discoideum interacts with the Hippo signaling pathway. Cell Cycle 2015, (in press).
78. Swift J., Discher D.E. The nuclear lamina is mechano-responsive to ECM elasticity in mature tissue. J. Cell Sci. 2014, 127:3005-3015.
79. Tanaka K. Intranuclear microtubule organizing center in early prophase nuclei of the plasmodium of the slime mold, Physarum polycephalum. J. Cell Biol. 1973, 57:220-224.
80. Tatout C., Evans D.E., Vanrobays E., Probst A.V., Graumann K. The plant LINC complex at the nuclear envelope. Chromosome Res. 2014, 22:241-252.
81. Tikhonenko I., Magidson V., Gräf R., Khodjakov A., Koonce M.P. A kinesin-mediated mechanism that couples centrosomes to nuclei. Cell. Mol. Life Sci. 2013, 70:1285-1296.
82. Ueda M., Schliwa M., Euteneuer U. Unusual centrosome cycle in Dictyostelium: correlation of dynamic behavior and structural changes. Mol. Biol. Cell 1999, 10:151-160.
83. Van Bortle K., Corces V.G. Spinning the web of cell fate. Cell 2013, 152:1213-1217.
84. Walker G., Dorrell R.G., Schlacht A., Dacks J.B. Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology 2011, 138:1638-1663.
85. Williams T.A., Foster P.G., Cox C.J., Embley T.M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 2013, 504:231-236.
86. Woese C.R., Kandler O., Wheelis M.L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:4576-4579.
87. Wright M., Albertini C., Planques V., Salles I., Ducommun B., Gely C., Akhavan Niaki H., Mir L., Moisand A., Oustrin M.L. Microtubule cytoskeleton and morphogenesis in the amoebae of the myxomycete Physarum polycephalum. Biol. Cell 1988, 63:239-248.
88. Xiong H., Rivero F., Euteneuer U., Mondal S., Mana-Capelli S., Larochelle D., Vogel A., Gassen B., Noegel A.A. Dictyostelium sun-1 connects the centrosome to chromatin and ensures genome stability. Traffic 2008, 9:708-724.
89. Zhang X., Lei K., Yuan X., Wu X., Zhuang Y., Xu T., Xu R., Han M. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009, 64:173-187.