Self-recognition and Ca2+-dependent carbohydrate-carbohydrate Cell adhesion provide clues to the cambrian explosion

Molecular Biology and Evolution

Volumn 26, Issue 11, 2009, Pages 2551-2561

  Fernández Busquets, Xavier ^a,b,c   Körnig, André ^a,b,d   Bucior, Iwona ^c,e   Burger, Max M ^c,f   Anselmetti, Dario ^d  

^a INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c MARINE BIOLOGICAL LABORATORY   (United States)

^d BIELEFELD UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Calcium; Cambrian explosion; Carbohydrates; Cell adhesion; Origin of Metazoa; Sponges

Indexed keywords

CALCIUM; CALCIUM ION; CARBOHYDRATE; SEA WATER;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CAMBRIAN; CELL ADHESION; EXPLOSION; GERM CELL; INHERITANCE; METAZOON; MOLECULAR RECOGNITION; MOLECULE; NONHUMAN; PRECAMBRIAN; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; EVOLUTION; METABOLISM; PHYSIOLOGY;

ANIMALIA; METAZOA;

ANIMALS; CALCIUM; CARBOHYDRATES; CELL ADHESION; EVOLUTION; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE;

EID: 73349125449     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp170     Document Type: Article

References (72)

1. Bell GI. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
2. Berner RA. 2004. A model for calcium, magnesium and sulfate in seawater over Phanerozoic time. Am J Sci. 304: 438-453.
3. Blumbach B, Diehl-Seifert B, Seack J, Steffen R, Müller IM, Müller WE. 1999. Cloning and expression of new receptors belonging to the immunoglobulin superfamily from the marine sponge Geodia cydonium. Immunogenetics. 49:751-763.
4. Brennan ST, Lowenstein TK, Horita J. 2004. Seawater chemistry and the advent of biocalcification. Geology. 32:473-476.
5. Bucior I, Burger MM. 2004. Carbohydrate-carbohydrate interaction as a major force initiating cell-cell recognition. Glycoconj J. 21:111-123. (Pubitemid 39382657)
6. Bucior I, Burger MM, Fernàndez-Busquets X. 2009. Carbohydrate-carbohydrate interactions. In: Gabius H-J, editor. The sugar code. Weinheim (Germany): WILEY-VCH Verlag GmbH & Co. KGaA. p. 347-362.
7. Bucior I, Scheuring S, Engel A, Burger MM. 2004. Carbohydrate- carbohydrate interaction provides adhesion force and specificity for cellular recognition. J Cell Biol. 165:529-537. (Pubitemid 38679618)
8. Budd GE. 2008. The earliest fossil record of the animals and its significance. Philos Trans R Soc Lond B Biol Sci. 363:1425-1434.
9. Buss LW. 1982. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA. 79:5337-5341.
10. Cauldwell CB, Henkart P, Humphreys T. 1973. Physical properties of sponge aggregation factor. A unique pro-teoglycan complex. Biochemistry. 12:3051-3055.
11. Chadwick-Furman NE, Weissman IL. 1995. Life history plasticity in chimaeras of the colonial ascidian Botryllus schlosseri. Proc R Soc Lond B. 262:157-162.
12. Conway-Morris S. 2006. Darwin's dilemma: the realities of the Cambrian 'explosion'. Philos Trans R Soc Lond B Biol Sci. 361:1069-1083.
13. Dammer U, Popescu O, Wagner P, Anselmetti D, Güntherodt HJ, Misevic GN. 1995. Binding strength between cell adhesion proteoglycans measured by atomic force microscopy. Science. 267:1173-1175.
14. Dawkins R. 1976. The selfish gene. Oxford: Oxford University Press.
15. Dunn CW, Hejnol A, Matus DQ, et al. (17 co-authors). 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 452:745-749.
16. Eckel R, Ros R, Decker B, Mattay J, Anselmetti D. 2005. Supramolecular chemistry at the single-molecule level. Angew Chem Int Ed Engl. 44:484-488.
17. Eggens I, Fenderson B, Toyokuni T, Dean B, Stroud M, Hakomori S. 1989. Specific interaction between Lex and Lex determinants. A possible basis for cell recognition in preimplantation embryos and in embryonal carcinoma cells. J Biol Chem. 264:9476-9484.
18. Elkinton JR. 1957. The relationship of water and salt. Proc Nutr Soc. 16:113-118.
19. Erdmann T, Schwarz US. 2004. Stochastic dynamics of adhesion clusters under shared constant force and with rebinding. J Chem Phys. 121:8997-9017.
20. Evans E, Ritchie K. 1997. Dynamic strength of molecular adhesion bonds. Biophys J. 72:1541-1555.
21. Feldgarden M, Yund PO. 1992. Allorecognition in colonial marine invertebrates: does selection favor fusion with kin or fusion with self? Biol Bull. 182:155-158.
22. Fernàndez-Busquets X. 2008. The sponge as a model of cellular recognition. In: Conn PM, editor. Sourcebook of models for biomedical research. Totowa (NJ): Humana Press Inc. p. 75-83.
23. Fernàndez-Busquets X, Burger MM. 1997. The main protein of the aggregation factor responsible for species-specific cell adhesion in the marine sponge Microciona prolifera is highly polymorphic. J Biol Chem. 272:27839-27847.
24. Fernàndez-Busquets X, Burger MM. 1999. Cell adhesion and histocompatibility in sponges. Microsc Res Tech. 44:204-218.
25. Fernàndez-Busquets X, Burger MM. 2003. Circular proteogly-cans from sponges: first members of the spongican family. Cell Mol Life Sci. 60:88-112.
26. Fernàndez-Busquets X, Gerosa D, Hess D, Burger MM. 1998. Accumulation in marine sponge grafts of the mRNA encoding the main proteins of the cell adhesion system. J Biol Chem. 273:29545-29553.
27. Fernàndez-Busquets X, Kuhns WJ, Simpson TL, Ho M, Gerosa D, Grob M, Burger MM. 2002. Cell adhesion-related proteins as specific markers of sponge cell types involved in allogeneic recognition. Dev Comp Immunol. 26:313-323.
28. Fritz J, Anselmetti D, Jarchow J, Fernàndez-Busquets X. 1997. Probing single biomolecules with atomic force microscopy. J Struct Biol. 119:165-171.
29. Garcia-Manyes S, Bucior I, Ros R, Anselmetti D, Sanz F, Burger MM, Fernàndez-Busquets X. 2006. Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans. J Biol Chem. 281: 5992-5999.
30. Gauthier M, Degnan BM. 2008. Partitioning of genetically distinct cell populations in chimeric juveniles of the sponge Amphimedon queenslandica. Dev Comp Immunol. 32:1270-1280.
31. Hakomori S. 1991. Carbohydrate-carbohydrate interaction as an initial step in cell recognition. Pure Appl Chem. 63: 473-482.
32. Hardie LA. 1996. Secular variation in seawater chemistry; an explanation for the coupled secular variation in the mineralogies of marine limestones and potash evaporites over the past 600 m.y. Geology. 24:279-283.
33. Hinterdorfer P, Baumgartner W, Gruber HJ, Schilcher K, Schindler H. 1996. Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc Natl Acad Sci USA. 93:3477-3481.
34. Humphreys T. 1963. Chemical dissolution and in vitro reconstruction of sponge cell adhesions. I. Isolation and functional demonstration of the components involved. Dev Biol. 8:27-47.
35. Hutter JL, Bechhofer J. 1993. Calibration of atomic force microscope tips. Rev Sci Instrum. 64:1868-1873.
36. Jarchow J, Fritz J, Anselmetti D, Calabro A, Hascall VC, Gerosa D, Burger MM, Fernàndez-Busquets X. 2000. Supramolecular structure of a new family of circular proteoglycans mediating cell adhesion in sponges. J Struct Biol. 132:95-105.
37. Jumblatt JE, Schlup V, Burger MM. 1980. Cell-cell recognition: specific binding of Microciona sponge aggregation factor to homotypic cells and the role of calcium ions. Biochemistry. 19:1038-1042.
38. Kerr RA. 2002. Paleoceanography. Inconstant ancient seas and life's path. Science. 298:1165-1166.
39. Knauth LP. 2005. Temperature and salinity history of the Precambrian ocean: implications for the course of microbial evolution. Palaeogeogr Palaeoclimatol Palaeoecol. 219:53-59.
40. Kruse M, Steffen R, Batel R, Müller IM, Müller WE. 1999. Differential expression of allograft inflammatory factor 1 and of glutathione peroxidase during auto-and allograft response in marine sponges. J Cell Sci. 112:4305-4313.
41. Kuusksalu A, Pihlak A, Müller WE, Kelve M. 1995. The (2#-5#)oligoadenylate synthetase is present in the lowest multicellular organisms, the marine sponges. Demonstration of the existence and identification of its reaction products. Eur J Biochem. 232:351-357.
42. Love GD, Grosjean E, Stalvies C, et al. (12 co-authors). 2009. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature. 457:718-721.
43. Lyubchenko Y, Shlyakhtenko L, Harrington R, Oden P, Lindsay S. 1993. Atomic force microscopy of long DNA: imaging in air and under water. Proc Natl Acad Sci USA. 90:2137-2140.
44. Maldonado M. 1998. Do chimeric sponges have improved chances of survival? Mar Ecol Prog Ser. 164:301-306.
45. Marshall CR. 2006. Explaining the Cambrian "explosion" of animals. Annu Rev Earth Planet Sci. 34:355-384.
46. Mathews CK, van Holde KE. 1990. Biochemistry. San Francisco (CA): The Benjamin/Cummings Publishing Company, Inc.
47. McGhee KE. 2006. The importance of life-history stage and individual variation in the allorecognition system of a marine sponge. J Exp Mar Biol Ecol. 333:241-250.
48. Misevic GN, Burger MM. 1993. Carbohydrate-carbohydrate interactions of a novel acidic glycan can mediate sponge cell adhesion. J Biol Chem. 268:4922-4929.
49. Misevic GN, Finne J, Burger MM. 1987. Involvement of carbohydrates as multiple low affinity interaction sites in the self-association of the aggregation factor from the marine sponge Microciona prolifera. J Biol Chem. 262:5870-5877.
50. Müller WE. 2001. How was metazoan threshold crossed? The hypothetical Urmetazoa. Comp Biochem Physiol A Mol Integr Physiol. 129:433-460.
51. Müller WE, Perovic S, Wilkesman J, Kruse M, Müller IM, Batel R. 1999. Increased gene expression of a cytokine-related molecule and profilin after activation of Suberites domuncula cells with xenogeneic sponge molecule(s). DNA Cell Biol. 18:885-893.
52. Müller WE, Schröder HC, Skorokhod A, Bünz C, Müller IM, Grebenjuk VA. 2001. Contribution of sponge genes to unravel the genome of the hypothetical ancestor of Metazoa (Urmetazoa). Gene. 276:161-173.
53. Müller WEG, Müller IM. 2003. Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol. 43:281-292.
54. Nursall JR. 1959. Oxygen as a prerequisite to the origin of the Metazoa. Nature. 183:1170-1172.
55. Pahler S, Blumbach B, Müller I, Müller WE. 1998. Putative multiadhesive protein from the marine sponge Geodia cydonium: cloning of the cDNA encoding a fibronectin-, an SRCR-, and a complement control protein module. J Exp Zool. 282:332-343.
56. Pancer Z, Skorokhod A, Blumbach B, Müller WE. 1998. Multiple Ig-like featuring genes divergent within and among individuals of the marine sponge Geodia cydonium. Gene. 207:227-233.
57. Peterson KJ, Cotton JA, Gehling JG, Pisani D. 2008. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc Lond B Biol Sci. 363:1435-1443.
58. Petrychenko OY, Peryt TM, Chechel EI. 2005. Early Cambrian seawater chemistry from fluid inclusions in halite from Siberian evaporites. Chem Geol. 219:149-161.
59. 2\+ required by the aggregation factor complex from the marine sponge, Microciona prolifera. J Biol Chem. 258:6394-6399.
60. Rinaudo M. 2006. Non-covalent interactions in polysaccharide systems. Macromol Biosci. 6:590-610.
61. Sabella C, Faszewski E, Himic L, Colpitts KM, Kaltenbach J, Burger MM, Fernàndez-Busquets X. 2007. Cyclosporin A suspends transplantation reactions in the marine sponge Microciona prolifera. J Immunol. 179:5927-5935.
62. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS. 2007. A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE. 2:e506.
63. Schwesinger F, Ros R, Strunz T, Anselmetti D, Güntherodt HJ, Honegger A, Jermutus L, Tiefenauer L, Pluckthun A. 2000. Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc Natl Acad Sci USA. 97:9972-9977.
64. Shen B, Dong L, Xiao S, Kowalewski M. 2008. The Avalon explosion: evolution of Ediacara morphospace. Science. 319:81-84.
65. Simkiss K. 1977. Biomineralization and detoxification. Calcif Tiss Res. 24:199-200.
66. Simpson TL. 1984. The cell biology of sponges. New York: Springer-Verlag.
67. Spillmann D, Burger MM. 1996. Carbohydrate-carbohydrate interactions in adhesion. J Cell Biochem. 61:562-568.
68. Steinberg MS, Garrod DR. 1975. Observations on the sorting-out of embryonic cells in monolayer culture. J Cell Sci. 18:385-403.
69. Stoner DS, Weissman IL. 1996. Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. Proc Natl Acad Sci USA. 93:15254-15259.
70. Valentine JW. 2004. On the origin of phyla. Chicago (IL): The University of Chicago Press.
71. Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WE. 2007. Toll-like receptors are part of the innate immune defense system of sponges (demospongiae: Porifera). Mol Biol Evol. 24:792-804.
72. Yu S, Kojima N, Hakomori SI, Kudo S, Inoue S, Inoue Y. 2002. Binding of rainbow trout sperm to egg is mediated by strong carbohydrate-to-carbohydrate interaction between (KDN)GM3 (deaminated neuraminyl ganglioside) and Gg3-like epitope. Proc Natl Acad Sci USA. 99: 2854-2859.