Evolution of an ancient protein function involved in organized multicellularity in animals

eLife

Volumn 5, Issue JANUARY2016, 2016, Pages

  Anderson, Douglas P ^a   Whitney, Dustin S ^b   Hanson Smith, Victor ^a,e   Woznica, Arielle ^c   Campodonico Burnett, William ^a   Volkman, Brian F ^b   King, Nicole ^c   Thornton, Joseph W ^d   Prehoda, Kenneth E ^a  

^a UNIVERSITY OF OREGON   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c University of California Berkeley   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; ANIMAL; CELL CYCLE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; SPINDLE APPARATUS;

CELL CYCLE PROTEIN; GUANYLATE KINASE; PROTEIN BINDING;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; EVOLUTION, MOLECULAR; GUANYLATE KINASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SPINDLE APPARATUS;

EID: 84956891086     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10147     Document Type: Article

References (61)

1. Agarwal KC, Miech RP, Parks RE. 1978. Guanylate kinases from human erythrocytes, hog brain, and rat liver. Methods Enzymol 51:483-490. doi: 10.1016/S0076-6879(78)51066-5.
2. Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O. 2011. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology 60:685-699. doi: 10.1093/sysbio/syr041.
3. Bell GP, Fletcher GC, Brain R, Thompson BJ. 2015. Aurora kinases phosphorylate lgl to induce mitotic spindle orientation in drosophila epithelia. Current Biology 25:61-68. doi: 10.1016/j.cub.2014.10.052.
4. Bergstralh DT, Lovegrove HE, St Johnston D. 2013. Discs large links spindle orientation to apical-basal polarity in drosophila epithelia. Current Biology 23:1707-1712. doi: 10.1016/j.cub.2013.07.017.
5. Bhabha G, Ekiert DC, Jennewein M, Zmasek CM, Tuttle LM, Kroon G, Dyson HJ, Godzik A, Wilson IA, Wright PE. 2013. Divergent evolution of protein conformational dynamics in dihydrofolate reductase. Nature Structural & Molecular Biology 20:1243-1249. doi: 10.1038/nsmb.2676.
6. Bilder D. 2000. Cooperative regulation of cell polarity and growth by drosophila tumor suppressors. Science 289:113-116. doi: 10.1126/science.289.5476.113.
7. Blaszczyk J, Li Y, Yan H, Ji X. 2001. Crystal structure of unligated guanylate kinase from yeast reveals GMP- induced conformational changes. Journal of Molecular Biology 307:247-257. doi: 10.1006/jmbi.2000.4427.
8. Bonner JT. 1998. The origins of multicellularity. Integrative Biology 1:27-36. doi: 10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6.
9. Bridgham JT. 2006. Evolution of hormone-receptor complexity by molecular exploitation. Science 312:97-101. doi: 10.1126/science.1123348.
10. Buss LW. 1988. The Evolution of Individuality. Princeton: Princeton University Press. doi: 10.1515/9781400858712.
11. Cabernard C, Doe CQ. 2009. Apical/Basal spindle orientation is required for neuroblast homeostasis and neuronal differentiation in drosophila. Developmental Cell 17:134-141. doi: 10.1016/j.devcel.2009.06.009.
12. Carroll SM, Bridgham JT, Thornton JW. 2008. Evolution of hormone signaling in elasmobranchs by exploitation of promiscuous receptors. Molecular Biology and Evolution 25:2643-2652. doi: 10.1093/molbev/msn204.
13. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate salpingoeca rosetta. Developmental Biology 357:73-82. doi: 10.1016/j.ydbio.2011.06.003.
14. de Mendoza A, Sebe-Pedros A, Ruiz-Trillo I. 2014. The evolution of the GPCR signaling system in eukaryotes: modularity, conservation, and the transition to metazoan multicellularity. Genome Biology and Evolution 6:606-619. doi: 10.1093/gbe/evu038.
15. de Mendoza A, Suga H, Ruiz-Trillo I. 2010. Evolution of the MAGUK protein gene family in premetazoan lineages. BMC Evolutionary Biology 10:93 doi: 10.1186/1471-2148-10-93.
16. De Smet I, Beeckman T. 2011. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nature Reviews Molecular Cell Biology 12:177-188. doi: 10.1038/nrm3064.
17. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792-1797. doi: 10.1093/nar/gkh340.
18. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen Min-yi, Pieper U, Sali A. 2006. Comparative protein structure modeling using modeller. Current Protocols in Bioinformatics:5.6.1-5.6.5. Chapter 5:Unit 5.6. doi: 10.1002/0471250953.bi0506s15.
19. Funke L, Dakoji S, Bredt DS. 2005. Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annual Review of Biochemistry 74:219-245. doi: 10.1146/annurev.biochem.74.082803.133339.
20. Gillies TE, Cabernard C. 2011. Cell division orientation in animals. Current Biology 21:R599-R609. doi: 10.1016/j.cub.2011.06.055.
21. Grosberg RK, Strathmann RR. 2007. The evolution of multicellularity: a minor major transition? Annual Review of Ecology 38:621-654. doi: 10.1146/annurev.ecolsys.36.102403.114735.
22. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307-321. doi: 10.1093/sysbio/syq010.
23. Hanada T. 2000. GAKIN, a novel kinesin-like protein associates with the human homologue of the drosophila discs large tumor suppressor in t lymphocytes. Journal of Biological Chemistry 275:28774-28784. doi: 10.1074/jbc.M000715200.
24. Hanson-Smith V, Kolaczkowski B, Thornton JW. 2010. Robustness of ancestral sequence reconstruction to phylogenetic uncertainty. Molecular Biology and Evolution 27:1988-1999. doi: 10.1093/molbev/msq081.
25. Harms MJ, Eick GN, Goswami D, Colucci JK, Griffin PR, Ortlund EA, Thornton JW. 2013. Biophysical mechanisms for large-effect mutations in the evolution of steroid hormone receptors. Proceedings of the National Academy of Sciences of the United States of America 110:11475-11480. doi: 10.1073/pnas.1303930110.
26. Harms MJ, Thornton JW. 2010. Analyzing protein structure and function using ancestral gene reconstruction. Current Opinion in Structural Biology 20:360-366. doi: 10.1016/j.sbi.2010.03.005.
27. Harms MJ, Thornton JW. 2013. Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nature Reviews Genetics 14:559-571. doi: 10.1038/nrg3540.
28. Horiguchi K. 2006. Transport of PIP3 by GAKIN, a kinesin-3 family protein, regulates neuronal cell polarity. The Journal of Cell Biology 174:425-436. doi: 10.1083/jcb.200604031.
29. Johnston CA, Doe CQ, Prehoda KE, Zhang Z. 2012. Structure of an enzyme-derived phosphoprotein recognition domain. PLoS ONE 7:e36014 doi: 10.1371/journal.pone.0036014.
30. Johnston CA, Hirono K, Prehoda KE, Doe CQ. 2009. Identification of an aurora-A/PinsLINKER/ dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell 138:1150-1163. doi: 10.1016/j.cell.2009.07.041.
31. Johnston CA, Whitney DS, Volkman BF, Doe CQ, Prehoda KE. 2011. Conversion of the enzyme guanylate kinase into a mitotic-spindle orienting protein by a single mutation that inhibits GMP-induced closing. Proceedings of the National Academy of Sciences of the United States of America 108:E973-E978. doi: 10.1073/pnas.1104365108.
32. King N, Young SL, Abedin M, Carr M, Leadbeater BSC. 2009. Starting and maintaining monosiga brevicollis cultures. Cold Spring Harbor Protocols 2009:pdb.prot5148. doi: 10.1101/pdb.prot5148.
33. King N. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361-363. doi: 10.1126/science.1083853.
34. King N. 2004. The unicellular ancestry of animal development. Developmental Cell 7:313-325. doi: 10.1016/j.devcel.2004.08.010.
35. Leadbeater BSC. 2015. The Choanoflagellates: Evolution, Biology and Ecology. Cambridge: Cambridge University Press. doi: 10.1017/CBO9781139051125.
36. Li Y, Zhang Y, Yan H. 1996. Kinetic and thermodynamic characterizations of yeast guanylate kinase. Journal of Biological Chemistry 271:28038-28044. doi: 10.1074/jbc.271.45.28038.
37. Lu MS, Johnston CA. 2013. Molecular pathways regulating mitotic spindle orientation in animal cells. Development 140:1843-1856. doi: 10.1242/dev.087627.
38. Maynard Smith J, Szathmary E. 1995. The Major Transitions in Evolution. Oxford: Oxford University Press.
39. Morin X, Bellaïche Y. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Developmental Cell 21:102-119. doi: 10.1016/j.devcel.2011.06.012.
40. Nakajima Y, Meyer EJ, Kroesen A, McKinney SA, Gibson MC. 2013. Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 500:359-362. doi: 10.1038/nature12335.
41. Nichols SA, Dirks W, Pearse JS, King N. 2006. Early evolution of animal cell signaling and adhesion genes. Proceedings of the National Academy of Sciences of the United States of America 103:12451-12456. doi: 10.1073/pnas.0604065103.
42. Nielsen C. 2008. Six major steps in animal evolution: are we derived sponge larvae? Evolution & Development 10:241-257. doi: 10.1111/j.1525-142X.2008.00231.x.
43. Richter DJ, King N. 2013. The genomic and cellular foundations of animal origins. Annual Review of Genetics 47: 509-537. doi: 10.1146/annurev-genet-111212-133456.
44. Rokas A. 2008. The molecular origins of multicellular transitions. Current Opinion in Genetics & Development 18: 472-478. doi: 10.1016/j.gde.2008.09.004.
45. Rokas A. 2008. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annual Review of Genetics 42:235-251. doi: 10.1146/annurev.genet.42.110807.091513.
46. Saadaoui M, Machicoane M, di Pietro F, Etoc F, Echard A, Morin X. 2014. Dlg1 controls planar spindle orientation in the neuroepithelium through direct interaction with LGN. The Journal of Cell Biology 206:707-717. doi: 10.1083/jcb.201405060.
47. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences of the united States of America 95:5857-5864. doi: 10.1073/pnas.95.11.5857.
48. Sebé-Pedrós A, Irimia M, Del Campo J, Parra-Acero H, Russ C, Nusbaum C, Blencowe BJ, Ruiz-Trillo I. 2013. Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2:e01287 doi: 10.7554/eLife.01287.
49. Sekulic N, Shuvalova L, Spangenberg O, Konrad M, Lavie A. 2002. Structural characterization of the closed conformation of mouse guanylate kinase. Journal of Biological Chemistry 277:30236-30243. doi: 10.1074/jbc.M204668200.
50. Siegrist SE, Doe CQ. 2005. Microtubule-induced Pins/Gai cortical polarity in drosophila neuroblasts. Cell 123: 1323-1335. doi: 10.1016/j.cell.2005.09.043.
51. Siegrist SE. 2006. Extrinsic cues orient the cell division axis in drosophila embryonic neuroblasts. Development 133:529-536. doi: 10.1242/dev.02211.
52. Smith NR, Prehoda KE. 2011. Robust spindle alignment in drosophila neuroblasts by ultrasensitive activation of pins. Molecular Cell 43:540-549. doi: 10.1016/j.molcel.2011.06.030.
53. te Velthuis AJW, Admiraal JF, Bagowski CP. 2007. Molecular evolution of the MAGUK family in metazoan genomes. BMC Evolutionary Biology 7:129 doi: 10.1186/1471-2148-7-129.
54. Tokuriki N, Tawfik DS. 2009. Protein dynamism and evolvability. Science 324:203-207. doi: 10.1126/science.1169375.
55. Trillo IR, Nedelcu AM. 2015. Evolutionary Transitions to Multicellular Life: Principles and Mechanisms (Advances in Marine Genomics). New York: Springer, New York.
56. Wang H, Oliferenko S, Balasubramanian MK. 2003. Cytokinesis: relative alignment of the cell division apparatus and the mitotic spindle. Current Opinion in Cell Biology 15:82-87. doi: 10.1016/S0955-0674(02)00006-6.
57. Williams SE, Beronja S, Pasolli HA, Fuchs E. 2011. Asymmetric cell divisions promote notch-dependent epidermal differentiation. Nature 470:353-358. doi: 10.1038/nature09793.
58. Woods DF. 1996. Dlg protein is required for junction structure, cell polarity, and proliferation control in drosophila epithelia. The Journal of Cell Biology 134:1469-1482. doi: 10.1083/jcb.134.6.1469.
59. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-1650.
60. Yoshiura S, Ohta N, Matsuzaki F. 2012. Tre1 GPCR signaling orients stem cell divisions in the drosophila central nervous system. Developmental Cell 22:79-91. doi: 10.1016/j.devcel.2011.10.027.
61. Zhu J, Shang Y, Xia C, Wang W, Wen W, Zhang M. 2011. Guanylate kinase domains of the MAGUK family scaffold proteins as specific phospho-protein-binding modules. The EMBO Journal 30:4986-4997. doi: 10.1038/emboj.2011.428.