Cnidarians: An evolutionarily conserved model system for regeneration?

Developmental Dynamics

Volumn 226, Issue 2, 2003, Pages 257-267

  Holstein, T W ^a   Hobmayer, E ^a,b   Technau, U ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Cnidaria; Hydra; Organizer; Regeneration; Self organisation; Wnt wg signaling

Indexed keywords

GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

CELL DIFFERENTIATION; COELENTERATE; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; EVOLUTION; FOOT; HEAT; METAZOON; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REGENERATION; REGENERATIVE ABILITY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION; VERTEBRATE;

ANIMALS; CNIDARIA; EVOLUTION; HEAD; REGENERATION; URODELA;

ANIMALIA; CNIDARIA; HYDRA; METAZOA; VERTEBRATA;

EID: 0037310204     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.10227     Document Type: Review

References (121)

1. Alder H, Schmid V, 1987, Cell cycles and in vitro transdifferentiation and regeneration of isolated striated muscle of jellyfish. Dev Biol 124:358-369.
2. Blitz IL, Shimmi O, Wunnenberg-Stapleton K, O'Connor MB, Cho KW, 2000. Is chordin a long-range- or short-range-acting factor? Roles for BMP1-related metalloproteases in chordin and BMP4 autofeedback loop regulation. Dev Biol 223:120-138.
3. Bode PM, Bode HR. 1984. Patterning in Hydra. In: Malacinski GM, Bryant SV, editors. Pattern formation. A primer in developmental biology. New York: Macmillan. p 213-241.
4. Bosch TCG, Fujisawa T. 2001, Polyps, peptides and patterning. Bioessays 23:420-427.
5. Bridge D, Cunningham CW, DeSalle R, Buss LW, 1995. Class-level relationship in the phylum Cnidaria: molecular and morphological evidence. Mol Biol Evol 12:679-689.
6. Brockes JBP, 1997. Amphibian limb regeneration: rebuilding a complex structure. Science 276:81-87.
7. Broun M, Bode HR. 2002, Characterization of the head organizer in Hydra. Development 129:875-884.
8. Broun M, Sokol S, Bode HR. 1999. Cngsc, a homologue of goosecold, participates in the patterning of the head, and is expressed in the organizer region of Hydra. Development 126:5245-5254.
9. Browne E. 1909. The production of new hydranths in Hydra by the insertion of small grafts. J Exp Biol 8:1-23.
10. Campbell RD. 7967a. Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of cell division. Dev Biol 15:487-502.
11. Campbell RD. 1967b. Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement. J Morphol 121:19-28.
12. Conway Morris S. 2000. The Cambrian "explosion": slow-fuse or megatonnage? Proc Natl Acad Sci U S A 97:4426-4429.
13. Cummings SG, Bode HR. 1984. Head regeneration and polarity reversal in Hydra attenuata can occur in the absence of DNA synthesis. Rouxs Arch Dev Biol 194:79-86.
14. David CN, Campbell RD. 1972. Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11:557-568.
15. David CN, Gierer A. 1974. Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359-375.
16. Day SJ, Lawrence PA, 2000. Measuring dimensions: the regulation of size and shape. Development 127:2977-2987.
17. DeRobertis EM, Bouwmeester T. 2001. New twists on embryonic patterning. EMBO Rep 2:661-665.
18. DeRobertis EM, Sasai Y. 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380:37-40.
19. Dudley AT, Ros MA, Tabin CJ. 2002. A re-examination of proximodistal patterning during vertebrate limb development. Nature 418:539-544.
20. Duboule D. 2002. Making progress with limb models. Nature 418:492-493.
21. Endl I, Lohmann JU, Bosch TCG. 1999. Head-specific gene expression in Hydra: complexity of DNA-protein interactions at the promoter of kas1 is inversely correlated to the head activation potential. Proc Natl Acad Sci U S A 96:1445-1450.
22. Entchev EV, Schwabedissen A, Gonzalez-Gaitan M. 2000. Gradient formation of the TGFbeta homolog Dpp. Cell 103:981-991.
23. Fagotto F, Gumbiner BM. 1996. Cell contact-dependent signaling. Dev Biol 180:445-454.
24. Forman BJ, Javois LC. 1999. Interactions between the foot and the head patterning systems in Hydra vulgaris. Dev Biol 210:351-366.
25. Fraser SE, Green CR, Bode HR, Gilula NB. 1987. Selective disruption of gap junctional communication interferes with a patterning process in hydra. Science 237:49-55.
26. Galceran J, Hsu SC, Grosschedl, R. 2001. Rescue of a Wnt mutation by an activated form of LEF-1: regulation of maintenance but not initiation of Brachyury expression. Proc Natl Acad Sci U S A 98:8668-8673.
27. Galliot B. 2000. Conserved and divergent genes in apex and axis development of cnidarians. Curr Opin Genet Dev 10:629-637.
28. Gardiner DM, Bryant SV. 1996. Molecular mechanisms in the control of limb regeneration: the role of homeobox genes. Int J Dev Biol 40:797-805.
29. Gardiner DM, Carlson MR, Roy S. 1999. Towards a functional analysis of limb regeneration. Semin Cell Dev Biol 10:385-393.
30. Glerer A, Meinhardt H. 1972. A theory of biological pattern formation. Kybernetik 12:30-39.
31. Gierer A, Berking S, Bode HR, David CN, Flick K, Hansmann G, Schaller H, Trenkner E. 1972. Regeneration of Hydra from reaggregated cells. Nature New Biol 239:98-101.
32. Gilbert SE. 2000. Developmental biology. Sunderland, MA: Sinauer Associates, Inc. 749 p.
33. Grawe F, Wodarz A, Lee B, Knust E, Skaer H. 1996. The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122:951-999.
34. Gurdon JB, Bourillot PY. 2001. Morphogen gradient interpretation. Nature 413:797-803.
35. Gurdon J, Lemaire P, Kato K. 1993. Community effects and related phenomena in development. Cell 75:831-834.
36. Hampe W, Urny J, Franke I, Hoffmeister-Ullerich SA, Herrmann D, Petersen CM, Lohmann J, Schaller HC. 1999. A head-activator binding protein is present in hydra in a soluble and a membrane-anchored form. Development 126:4077-4086.
37. Harland R, Gerhart, J. 1997. Formation and function of Spemann's organizer. Annu Rev Cell Dev Biol 13:611-667.
38. Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE. 2002. Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci U S A 99:8106-8111.
39. Hicklin J, Wolpert L. 1973. Positional information and pattern regulation in hydra: the effect of gamma-radiation. J Embryol Exp Morphol 30:741-752.
40. Hobmayer B, Holstein TW, David CN. 1997. Stimulation of tentacle and bud formation by the neuropeptide head activator in Hydra magnipapillata. Dev Biol 183:1-8.
41. Hobmayer B, Rentzsch F, Kuhn K, Happel CM, Laue C, Snyder P, Rothbächer U, Holstein, TW, 2000. Wnt signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186-189.
42. Hobmayer B, Rentzsch F, Holstein TW, 2001a. Identification and expression of HySmadl, a member of the R-Smad family of TGF-beta signal transducers, in the diploblastic metazoan Hydra. Deve Genes Evol 211:597-602.
43. Hobmayer B, Snyder P, Alt D, Happel C, Holstein TW. 2001b. Quantitative analysis of epithelial cell aggregation in the diploblastic metazoan Hydra reveals a switch from homotypic to heterotypic interactions. Cell Tissue Res 304:147-157.
44. Hoffmeister SAH, Schaller HC. 1985. A new biochemical marker for foot-specific cell differentiation in hydra. Rouxs Arch Dev Biol 194:453-461.
45. Holstein TW, David CN. 1990. Putative intermediates in the nerve cell differentiation pathway in hydra have properties of multipotent stem cells. Dev Biol 142:401-405.
46. Holstein TW, Hobmayer E, David CN. 1991. Pattern of epithelial cell cycling in Hydra. Dev Biol 148:602-611.
47. Javois LC, Frazier-Edwards AM. 1991. Simultaneous effects of head activator on the dynamics of apical and basal regeneration in Hydra vulgaris (formerly Hydra attenuata). Dev Biol 144:78-85.
48. Kishimoto Y, Murate M, Sugiyama T. 1996. Hydra regeneration from recombined ectodermal and endodermal tissue. I. Epibolic ectodermal spreading is driven by cell intercalation. J Cell Sci 109:763-772.
49. Knoll AH, Carroll SB. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284:2129-2137.
50. Lawrence PA. 2001. Wingless signalling: more about the Wingless morphogen. Curr Biol 11:R638-R639.
51. Lee PC, Javois LC. 1993. Patterning of heads and feet during regeneration of Hydra oligactis aggregates. Dev Biol 157:10-18.
52. Lelong C, Mathieu M, Favrel P. 2001. Identification of new bone morphogenetic protein-related members in invertebrates. Biochimie 83:423-426.
53. Lenhoff HM. 1991. Ethel Browne, Hans Spemann, and the discovery of the organizer phenomenon. Biol Bull 181:72-80.
54. Lessing D, Nusse R. 1998. Expression of wingless in the Drosophila embryo: a conserved cis-acting element lacking conserved Ci-binding sites is required for patched-mediated repression. Development 125:1469-1476.
55. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22:361-365.
56. Lo DC, Allen F, Brockes JP. 1993. Reversal of muscle differentiation during urodele limb regeneration. Proc Natl Acad Sci U S A 90:7230-7234.
57. MacWilliams HK. 1982. Numerical simulations of Hydra head regeneration using a proportion-regulating version of the Gierer-Meinhardt model. J Theor Biol 99:681-703.
58. MacWilliams HK. 1983a. Hydra transplantation phenomena and the mechanism of Hydra head regeneration. I. Properties of the head inhibition. Dev Biol 96:217-238.
59. MacWilliams HK. 1983b. Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of head activation. Dev Biol 96:239-257.
60. Marcum BA, Campbell RD, Romero J. 1977. Polarity reversal in nerve-free Hydra. Science 197:771-773.
61. Martinez DE, Dirksen ML, Bode PM, Jamrich M, Steele RE, Bode HR. 1997. Budhead, a forkhead/HNF-3 homologue, is expressed during axis formation and head specification in Hydra. Dev Biol 192:523-536.
62. Meinhardt H. 1982. Models of biological pattern formation. London: Academic Press.
63. Meinhardt H. 1993. A model for pattern formation of hypostome, tentacles, and foot in Hydra: how to form structures close to each other, how to form them at a distance, Dev Biol 157:321-333.
64. Minobe S, Fei K, Yan L, Sarras MP, Werle MJ. 2000. Identification and characterization of the epithelial polarity receptor "Frizzled" in Hydra vulgaris. Dev Genes Evol 210:258-262.
65. Müller WA. 1990 Ectopic head and foot formation in Hydra: diacylglycerol-induced increase in positional value and assistance of the head in foot formation. Differentiation 42:131-143.
66. Müller WA, 1995. Competition for factors and cellular resources as a principle of pattern formation in Hydra. II. Assistance of foot formation by heads and buds and a new model of pattern control. Dev Biol 167:175-189.
67. Müller WA. 1996. Head formation at the basal end and mirror-image pattern duplication in Hydra vulgaris. Int J Dev Biol 40:1119-1131.
68. Müller P, Yanze N, Schmid V, Spring J. 1999. The homeobox gene Otx of the jellyfish Podocoryne carnea: role of a head gene in striated muscle and evolution. Dev Biol 216:582-594.
69. Murate M, Kishimoto Y, Sugiyama T, Fujisawa T, Takahashi-Iwanaga H, Iwanaga T. 1997. Hydra regeneration from recombined ectodermal and endodermal tissue. II. Differential stability in the ectodermal and endodermal epithelial organization. J Cell Sci 110:1919-1934.
70. Mutz E. 1930. Transplantationsversuche an Hydra mit besonderer Berücksichtigung der Induktion. Regionalität und Polarität. Arch Entwicklungsmechanik Org 121:210-271.
71. Nielsen C. 2001. Animal evolution: interrelationships of the living phyla. New York: Oxford University Press. 480 p.
72. Noda K. 1971. Reconstitution of dissociated cells of Hydra. Zool Mag 80:27-31.
73. Noda K, Egami N. 1975. Regeneration of transplanted intact cell populations in lethally irradiated hydra. Radiat Res 63:174-184.
74. Otto JJ, Campbell RD. 1977. Budding in Hydra attenuata: bud stages and fate map. J Exp Zool 200:417-428.
75. Park HD, Ortmeyer AB, Blankenbaker DP. 1970. Cell division during regeneration in Hydra. Nature 227:617-619.
76. Petersen KW, Eernisse DJ. 2001. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol Dev 3:170-205.
77. Reber-Muller S, Spissinger T, Schuchert P, Spring J, Schmid V. 1995. An extracellular matrix protein of jellyfish homologous to mammalian fibrillins forms different fibrils depending on the life stage of the animal. Dev Biol 169:662-672.
78. Samuel G, Miller D, Saint R, 2001. Conservation of a DPP/BMP signalling pathway in the nonbilateral cnidarian Acropora millepora. Evol Dev 3:241-250.
79. Sarras MP Jr, Meador D, Zhang XM. 1991. Extracellular matrix (mesoglea) of Hydra vulgaris. II. Influence of collagen and components on head regeneration. Dev Biol 148:495-500.
80. Sarras MP Jr, Zhang X, Huff JK, Accavitti MA, St John PL, Abrahamson DR. 1993. Extracellular matrix (mesoglea) of Hydra vulgaris III. Formation and function during morphogenesis of hydra cell aggregates. Dev Biol 157:383-398.
81. Sato M, Tashiro H, Oikawa A, Sawada Y. 1992. Patterning in hydra cell aggregates without the sorting of cells from different axial origins. Dev Biol 151:111-116.
82. Sato-Maeda M, Uchida M, Graner F, Tashiro H. 1994. Quantitative evaluation of tissue-specific cell adhesion at the level of a single cell pair. Dev Biol 162:77-84.
83. Schaller HC. 1973, Isolation and characterization of a low-molecular-weight substance activating head and bud formation in hydra. J Embryol Exp Morphol 29:27-38.
84. Schaller HC. 1976. Action of the head activator as a growth hormone in hydra. Cell Differ 5:1-11.
85. Schaller HC, Flick K, Darai G. 1977. A neurohormone from hydra is present in brain and intestine of rat embryos. J Neurochem 29:393-394.
86. Schaller HC, Hofmann M, Javois LC. 1990. Effect of head activator on proliferation, head-specific determination and differentiation of epithelial cells in hydra. Differentiation 43:157-164.
87. Schiliro DM, Forman BJ, Javois LC. 1999. Interactions between the foot and bud patterning systems in Hydra vulgaris. Dev Biol 209:399-408.
88. Schmid V. 1992. Transdifferentiation in medusae. Int Rev Cytol 142:213-261.
89. Schmid V, Reber-Muller S. 1995. Transdifferentiation of isolated striated muscle of jellyfish in vitro: the initiation process. Semin Cell Biol 6:109-116.
90. Schmid V, Yanze N, Spring J, Reber-Müller S. 1998. The striated muscle of hydrozoan medusae: development and stability of the differentiated state. Zool-Anal Complex Syst 101:365-374.
91. Shilo BZ. 2001. The organizer and beyond. Cell 106:17-22.
92. Shimizu H, Zhang X, Zhang J, Leontovich A, Fei K, Yan L, Sarras MP Jr. 2002. Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 129:1521-1532.
93. Spemann H, Mangold H. 1924. Über die Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Arch Mikrosk Anat Entwicklungs 100:599-638.
94. Spring J, Yanze N, Middel AM, Stierwald M, Groger H, Schmid V. 2000. The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228:363-375.
95. Srinivasan S, Rashka KE, Bier E. 2002. Creation of a Sog morphogen gradient in the Drosophila embryo. Dev Cell 2:91-101.
96. Stocum DL. 2001. Stem cells in regenerative biology and medicine. Wound Repair Regen 9:429-442.
97. Suga H, Ono K, Miyata T. 1999. Multiple TGF-beta receptor related genes in sponge and ancient gene duplications before the parazoan-eumetazoan split. FEBS Lett 453:346-350.
98. Sun X, Mariani FV, Martin GR. 2002. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501-508.
99. Tada M, Smith JC. 2000. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127:2227-2238.
100. Tada M, Casey ES, Fairclough L, Smith JC. 1998. Blx1, a direct target of Xenopus T-box genes causes formation of ventral mesoderm and endoderm. Development 125:3997-4006.
101. Takahashi T, Muneoka Y, Lohmann J, deHaro LM, Solleder G, Bosch TCG, David CN, Bode HR, Koizumi O, Shimizu H, Hatta M, Fujisawa T, Sugiyama T. 1997. Systematic isolation of peptide signal molecules regulating development in hydra: Lwamide and PW families. Proc Natl Acad Sci U S A 94:1241-1246.
102. Takahashi H, Hotta K, Erives A, Di Gregorio A, Zeller RW, Levine M, Satoh N. 1999. Brachyury downstream notochord differentiation in the ascidian embryo. Genes Dev 13:1519-1523.
103. Tardent P, 1978. Coelenterata, Cnidaria. In: Seidel F, editor. Morphogenese der Tiere. Lf1: I Cnidaria. Jena/Stuttgart: Fischer Verlag. p 1-415.
104. Technau U, Bode HR. 1999. HyBra1, a brachyury homologue, acts during head formation in Hydra. Development 126:999-1010.
105. Technau U, Holstein TW. 1992. Cell sorting during the regeneration of Hydra from reaggregated cells. Dev Biol 151:117-127.
106. Technau U, Holstein TW. 1995. Head formation in Hydra is different at apical and basal levels. Development 121:1273-1282.
107. Technau U, Cramer von Laue C, Rentzsch F, Luft S, Hobmayer B, Bode HR, Holstein TW. 2000. Parameters of self-organisation in Hydra aggregates, Proc Natl Acad Sci U S A 97:12127-12131.
108. Turing A. 1952. The chemical basis of morphogenesis. Philos Trans R Soc London B 237:37-72.
109. Van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789-799.
110. Webster G. 1966a. Studies on pattern regulation in hydra. III. Dynamic aspects of factors controlling hypostome formation. J Embryol Exp Morphol 16:123-141.
111. Webster G. 1966b. Studies on pattern regulation in hydra. II. Factors controlling hypostome formation. J Embryol Exp Morphol 16:105-122.
112. Webster G, Wolpert L. 1966. Studies on pattern regulation in hydra. I. Regional differences in time required for hypostome determination. J Embryol Exp Morphol 16:91-104.
113. Wilby OK, Webster G. 1970a. Experimental studies on axial polarity in hydra. J Embryol Exp Morphol 24:595-613.
114. Wilby OK, Webster G. 1970b. Studies on the transmission of hypostome inhibition in hydra. J Embryol Exp Morphol 24:583-593.
115. Wolpert L. 2002. Principles of development. 2nd ed. New York: Oxford University Press. 542 p.
116. Wolpert L, Hicklin J, Hornbruch A. 1971. Positional information and pattern regulation in regeneration of hydra. Symp Soc Exp Biol 25:391-415.
117. Wolpert L, Clarke MRB, Hornbruch A. 1972. Positional signaling in Hydra. Nat New Biol 239:101-105.
118. Yan L, Pollock GH, Nagase H, Sarras MP Jr. 1995. A 25.7 × 10(3) M(r) hydra metalloproteinase (HMP1), a member of the astacin family, localizes to the extracellular matrix of Hydra vulgaris in a head-specific manner and has a developmental function. Development 121:1591-1602.
119. Yan L, Leontovich A, Fei K, Sarras MP Jr. 2000. Hydra metalloproteinase 1: a secreted astacln metalloproteinase whose apical axis expression is differentially regulated during head regeneration. Dev Biol 219:115-128.
120. Yanze N, Groger H, Muller P, Schmid V. 1999. Reversible inactivation of cell type-specific regulatory and structural genes in migrating isolated striated bxmuscle cells of jellyfish. Dev Biol 216:582-94.
121. Yao, T. 1945. Studies on the organizer problem in Pelmatohydra oligactis. I. The induction potency of the implants and the nature of the induced hydranth. J Exp Biol 21:147-150.