An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity

BioEssays

Volumn 34, Issue 10, 2012, Pages 833-840

  Dickinson, Daniel J ^a,b   Nelson, W James ^a   Weis, William I ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Dictyostelium; Epithelium; Metazoan evolution; Multicellularity

Indexed keywords

ALPHA CATENIN; BETA CATENIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; RIBOSOME RNA;

ACANTHAMOEBA; ANIMAL; ARTICLE; BIODIVERSITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL JUNCTION; CELL MOTION; CELL POLARITY; CELL STRUCTURE; CHEMOTAXIS; CHOANOFLAGELLATE; COLONY FORMATION; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; EPITHELIUM; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEEDING; FORCE; FUNGUS; LIFE CYCLE STAGE; MORPHOGENESIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; REPRODUCTION; RNA SEQUENCE; WNT SIGNALING PATHWAY;

ANIMALS; BIOLOGICAL EVOLUTION; CELL POLARITY; DICTYOSTELIUM; EPITHELIAL CELLS; EPITHELIUM; HUMANS;

ANIMALIA; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; FUNGI; METAZOA;

EID: 84866269357     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201100187     Document Type: Article

References (53)

1. Marchiando AM, Graham WV, Turner JR. 2010. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 5: 119- 44.
2. Bryant DM, Mostov KE. 2008. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9: 887- 901.
3. Tanos B, Rodriguez-Boulan E. 2008. The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27: 6939- 57.
4. St Johnston D, Sanson B. 2011. Epithelial polarity and morphogenesis. Curr Opin Cell Biol 23: 540- 6.
5. Nichols SA, Dirks W, Pearse JS, King N. 2006. Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103: 12451- 6.
6. Fahey B, Degnan BM. 2010. Origin of animal epithelia: insights from the sponge genome. Evol Dev 12: 601- 17.
7. Nelson WJ. 2003. Adaptation of core mechanisms to generate cell polarity. Nature 422: 766.
8. Shapiro L, Weis WI. 2009. Structure and biochemistry of cadherins and catenins. Cold Spring Harb Perspect Biol 1: a003053.
9. Nelson WJ. 2008. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem Soc Trans 36: 149- 55.
10. Steenkamp ET, Wright J, Baldauf SL. 2006. The protistan origins of animals and fungi. Mol Biol Evol 23: 93- 106.
11. Baldauf SL. 2003. The deep roots of eukaryotes. Science 300: 1703- 6.
12. King N. 2004. The unicellular ancestry of animal development. Dev Cell 7: 313- 25.
13. Medina M, Collins AG, Taylor JW, Valentine JW, et al. 2003. Phylogeny of opisthokonta and the evolution of multicellularity and complexity in fungi and metazoa. Int J Astrobiol 2: 203- 11.
14. Tyler S. 2003. Epithelium-the primary building block for metazoan complexity. Integr Comp Biol 43: 55- 63.
15. Dickinson DJ, Nelson WJ, Weis WI. 2011. A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins. Science 331: 1336- 9.
16. Dickinson DJ, Robinson DN, Nelson WJ, Weis WI. 2012. α-Catenin and IQGAP1 regulate myosin localization to control epithelial tube morphogenesis in Dictyostelium. Dev Cell, in press, DOI: 10.1016/j.devcel.2012.06.008.
17. Urushihara H. 2008. Developmental biology of the social amoeba: history, current knowledge and prospects. Dev Growth Differ 50: S277- 81.
18. Kessin RH. 2001. Dictyostelium. Cambridge: Cambridge University Press.
19. Harrington BJ, Raper KB. 1968. Use of a fluorescent brightener to demonstrate cellulose in the cellular slime molds. Appl Microbiol 16: 106- 13.
20. McRobbie SJ, Tilly R, Blight K, Ceccarelli A, et al. 1988. Identification and localization of proteins encoded by two DIF-inducible genes of Dictyostelium. Dev Biol 125: 59- 63.
21. Raper KB, Fennell DI. 1952. Stalk formation in Dictyostelium. B Torrey Bot Club 79: 25- 51.
22. Bonner JT. 1944. A descriptive study of the development of the slime mold Dictyostelium discoideum. Am J Bot 31: 175- 82.
23. Bonner JT, Cihiquoine AD, Kolderie MQ. 1955. A histochemical study of differentiation in the cellular slime molds. J Exp Zool 130: 133- 58.
24. Dormann D, Siegert F, Weijer CJ. 1996. Analysis of cell movement during the culmination phase of Dictyostelium development. Development 122: 761- 9.
25. Grimson MJ, Coates JC, Reynolds JP, Shipman M, et al. 2000. Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism. Nature 408: 727- 31.
26. George RP, Hohl HR, Raper KB. 1972. Ultrastructural development of stalk-producing cells in dictyostelium discoideum, a cellular slime mould. J Gen Microbiol 70: 477- 89.
27. Hohl HR, Hamamoto ST, Hemmes DE. 1968. Ultrastructural aspects of cell elongation, cellulose synthesis, and spore differentiation in Acytostelium leptosomum, a cellular slime mold. Am J Bot 55: 783- 96.
28. Schaap P, van der Molen L, Konijn TM. 1983. The organisation of fruiting body formation in Dictyostelium minutum. Cell Differ 12: 287- 97.
29. Schaap P, Pinas J, Wang M. 1985. Patterns of cell differentiation in several cellular slime mold species. Dev Biol 111: 51- 61.
30. Schaap P, Winckler T, Nelson M, Alvarez-Curto E, et al. 2006. Molecular phylogeny and evolution of morphology in the social amoebas. Science 314: 661- 3.
31. Goldstein B, Macara IG. 2007. The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13: 609- 22.
32. Clevers H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127: 469- 80.
33. Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, et al. 2010. Integration of contractile forces during tissue invagination. J Cell Biol 188: 735- 49.
34. Dawes-Hoang RE, Parmar KM, Christiansen AE, Phelps CB, et al. 2005. Folded gastrulation, cell shape change and the control of myosin localization. Development 132: 4165- 78.
35. Kuroda S, Fukata M, Nakagawa M, Fujii K, et al. 1998. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science 281: 832- 5.
36. Li Z, Kim SH, Higgins JM, Brenner MB, et al. 1999. IQGAP1 and calmodulin modulate E-cadherin function. J Biol Chem 274: 37885- 92.
37. Yamashiro S, Abe H, Mabuchi I. 2007. IQGAP2 is required for the cadherin-mediated cell-to-cell adhesion in Xenopus laevis embryos. Dev Biol 308: 485- 93.
38. Raper KB. 1984. The Dictyostelids. Princeton: Princeton University Press.
39. Brown MW, Spiegel FW, Silberman JD. 2009. Phylogeny of the "forgotten" cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol 26: 2699- 709.
40. King N, Hittinger CT, Carroll SB. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361- 3.
41. King N, Westbrook MJ, Young SL, Kuo A, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783- 8.
42. Ruiz-Trillo I, Lane CE, Archibald JM, Roger AJ. 2006. Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53: 379- 84.
43. Abedin M, King N. 2008. The premetazoan ancestry of cadherins. Science 319: 946- 8.
44. Knoll AH, Carroll SB. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284: 2129- 37.
45. Berney C, Pawlowski J. 2006. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc Biol Sci 273: 1867- 72.
46. Olive EW. 1902. Monograph of the Acrasieae. Proc Boston Soc Nat Hist 30: 451- 513.
47. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, et al. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357: 73- 82.
48. Paps J, Ruiz Trillo I. 2010. Animals and their unicellular ancestors. In Encyclopedia of Life Sciences. Chichester: John Wiley & Sons, Ltd.
49. Ruiz-Trillo I, Burger G, Holland PWH, King N, et al. 2007. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 23: 113- 8.
50. Sánchez-Martínez C, Pérez-Martín J. 2001. Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis-similar inputs, different outputs. Curr Opin Microbiol 4: 214- 21.
51. Grosberg RK, Strathmann RR. 2007. The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38: 621- 54.
52. Srivastava M, Simakov O, Chapman J, Fahey B, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720- 6.
53. King N, Young S, Abedin M, Carr M, et al. 2009. The choanoflagellates: heterotrophic nanoflagellates and sister group of the metazoa. Cold Spring Harb Protoc 2009: pdb.emo116.