Head regeneration in Hydra

Hydra, a primitive metazoan, has a simple structure consisting of a head, body column, and foot aligned along a single oral–aboral axis. The body column has a high capacity for regeneration of both the head and foot. Because of the tissue dynamics that take place in adult Hydra, the processes governing axial patterning are continuously active to maintain the form of the animal. Regeneration in hydra is morphallactic and closely related to these axial patterning processes. As might be expected, analysis at the molecular level indicates that the same set of genes are involved in head regeneration and the maintenance of the head in the context of the tissue dynamics of the adult. The genes analyzed so far play roles in axial patterning processes in bilaterians. Developmental Dynamics 226:225–236, 2003. © 2003 Wiley‐Liss, Inc.

[1]  H. Schaller,et al.  A new biochemical marker for foot-specific cell differentiation in hydra , 1985, Wilhelm Roux's archives of developmental biology.

[2]  M. Hatta,et al.  Enhancement of foot formation in Hydra by a novel epitheliopeptide, Hym-323. , 2001, Development.

[3]  H. Schaller,et al.  Isolation and characterization of a low-molecular-weight substance activating head and bud formation in hydra. , 1973, Journal of embryology and experimental morphology.

[4]  R. D. Campbell,et al.  Development of Hydra lacking nerve and interstitial cells. , 1978, Journal of cell science.

[5]  H. Bode,et al.  CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. , 1996, Developmental biology.

[6]  R. Boot-Handford,et al.  Molecular, biochemical and functional analysis of a novel and developmentally important fibrillar collagen (Hcol-I) in hydra. , 2000, Development.

[7]  M. Hassel,et al.  Pattern formation in Hydra vulgaris is controlled by lithium-sensitive processes. , 1993, Developmental biology.

[8]  A. Gierer,et al.  Regeneration of hydra from reaggregated cells. , 1972, Nature: New biology.

[9]  H. Bode,et al.  Development of the two-part pattern during regeneration of the head in hydra. , 1988, Development.

[10]  H. Theisen,et al.  Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs. , 1997, Development.

[11]  H. Macwilliams.  Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. , 1983, Developmental biology.

[12]  O K Wilby,et al.  Studies on the transmission of hypostome inhibition in hydra. , 1970, Journal of embryology and experimental morphology.

[13]  H. Schaller,et al.  Differentiation pathways of ectodermal epithelial cells in hydra. , 1987, Differentiation; research in biological diversity.

[14]  H. Bode,et al.  The novel signal peptides, pedibin and Hym-346, lower positional value thereby enhancing foot formation in hydra. , 1999, Development.

[15]  W. Müller,et al.  Ectopic head and foot formation in Hydra: diacylglycerol-induced increase in positional value and assistance of the head in foot formation. , 1990, Differentiation; research in biological diversity.

[16]  S. Berking,et al.  In the multiheaded strain (mh‐1) of Hydra magnipapillata the ectodermal epithelial cells are responsible for the formation of additional heads and the endodermal epithelial cells for the reduced ability to regenerate a foot , 2002, Development, growth & differentiation.

[17]  H. Bode,et al.  Head regeneration and polarity reversal inHydra attenuata can occur in the absence of DNA synthesis , 1984, Wilhelm Roux's archives of developmental biology.

[18]  G L Snyder,et al.  Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. , 2000, European journal of biochemistry.

[19]  M. Hatta,et al.  Identification of a Hydra homologue of the beta-catenin/plakoglobin/armadillo gene family. , 1996, Gene.

[20]  T. Holstein,et al.  Pattern of epithelial cell cycling in hydra. , 1991, Developmental biology.

[21]  O K Wilby,et al.  Experimental studies on axial polarity in hydra. , 1970, Journal of embryology and experimental morphology.

[22]  R. Boot-Handford,et al.  Characterization of Hydra Type IV Collagen , 2000, The Journal of Biological Chemistry.

[23]  Isolation and amino acid sequence of a morphogenetic peptide from hydra. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. , 1972, Journal of cell science.

[25]  L. Wolpert,et al.  Positional information and pattern regulation in regeneration of hydra. , 1971, Symposia of the Society for Experimental Biology.

[26]  H. Bode,et al.  CnOtx, a member of the Otx gene family, has a role in cell movement in hydra. , 1999, Developmental biology.

[27]  H. Bode,et al.  HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. , 2000, Development.

[28]  A. Leontovich,et al.  Hydra metalloproteinase 1: a secreted astacin metalloproteinase whose apical axis expression is differentially regulated during head regeneration. , 2000, Developmental biology.

[29]  H. Schaller,et al.  Head activator and head inhibitor are signals for nerve cell differentiation in hydra , 1987 .

[30]  T. Fujisawa,et al.  Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. , 1978, Journal of cell science.

[31]  H. Schaller,et al.  Effect of head activator on proliferation, head-specific determination and differentiation of epithelial cells in hydra. , 1990, Differentiation; research in biological diversity.

[32]  T. Holstein,et al.  Tentacle morphogenesis in hydra I. The role of head activator , 1990 .

[33]  Ethel Nicholson Browne,et al.  The production of new hydranths in Hydra by the insertion of small grafts , 1909 .

[34]  F. McCormick,et al.  Wnt Signaling to β-Catenin Involves Two Interactive Components , 2000, The Journal of Biological Chemistry.

[35]  R. D. Campbell.  Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement , 1967, Journal of morphology.

[36]  P. Tardent,et al.  The influences of ecto- and endoderm in determining the axial polarity ofHydra attenuata Pall. (Cnidaria, Hydrozoa) , 2004, Wilhelm Roux's archives of developmental biology.

[37]  P M Bode,et al.  Formation of pattern in regenerating tissue pieces of hydra attenuata. I. Head-body proportion regulation. , 1980, Developmental biology.

[38]  H. Bode.  The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. , 1996, Journal of cell science.

[39]  T. Holstein,et al.  Head formation in Hydra is different at apical and basal levels , 1995 .

[40]  Christoph M. Happel,et al.  WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra , 2000, Nature.

[41]  H. Bode,et al.  HyBra1, a Brachyury homologue, acts during head formation in Hydra. , 1999, Development.

[42]  H. Bode,et al.  Patterning of the head in hydra as visualized by a monoclonal antibody. I. Budding and regeneration. , 1986, Developmental biology.

[43]  H. Meinhardt.  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. , 1993, Developmental biology.

[44]  H. Schaller.  Head activator controls head formation in reaggregated cells of hydra , 1975 .

[45]  H. Schaller.  Action of the head activator as a growth hormone in hydra. , 1976, Cell differentiation.

[46]  Y Sawada,et al.  Minimum tissue size required for hydra regeneration. , 1993, Developmental biology.

[47]  T. Sugiyama,et al.  Genetic analysis of developmental mechanisms in hydra. X. Morphogenetic potentials of a regeneration-deficient strain (reg-16). , 1985, Developmental biology.

[48]  T. Fujisawa,et al.  GENETIC ANALYSIS OF DEVELOPMENTAL MECHANISMS IN HYDRA I. SEXUAL REPRODUCTION OF HYDRA MAGNIPAPILLATA AND ISOLATION OF MUTANTS , 1977, Development, growth & differentiation.

[49]  E. Kobatake,et al.  Genetic analysis of developmental mechanisms in hydra. XIX. Stimulation of regeneration by injury in the regeneration-deficient mutant strain, reg-16. , 1989, Development.

[50]  E. Boncinelli,et al.  From fly head to mammalian forebrain: the story of otd and Otx. , 1994, Trends in genetics : TIG.

[51]  H. Schaller,et al.  Role of the neuropeptide head activator for growth and development in hydra and mammals. , 1989, Development.

[52]  H. Bode,et al.  Formation of pattern in regenerating tissue pieces of Hydra attenuata. II. Degree of proportion regulation is less in the hypostome and tentacle zone than in the tentacles and basal disc. , 1984, Developmental biology.

[53]  A. Leontovich,et al.  Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. , 2002, Development.

[54]  J. Lengyel,et al.  It takes guts: the Drosophila hindgut as a model system for organogenesis. , 2002, Developmental biology.

[55]  N. A. Stover,et al.  Expression of a novel receptor tyrosine kinase gene and a paired-like homeobox gene provides evidence of differences in patterning at the oral and aboral ends of hydra. , 2000, Developmental biology.

[56]  S. Bhassu.  genbank accession numbers , 2004 .

[57]  H. Bode,et al.  Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  R. D. Campbell,et al.  Tissue economics of hydra: regulation of cell cycle, animal size and development by controlled feeding rates. , 1977, Journal of cell science.

[59]  H. Macwilliams.  Hydra transplantation phenomena and the mechanism of Hydra head regeneration: II. Properties of the head activation , 1983 .

[60]  H. Bode,et al.  Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra. , 1999, Development.

[61]  A. Leontovich,et al.  A novel hydra matrix metalloproteinase (HMMP) functions in extracellular matrix degradation, morphogenesis and the maintenance of differentiated cells in the foot process. , 2000, Development.

[62]  S. Berking,et al.  Lithium ions interfere with pattern control in Hydra vulgaris , 1990, Roux's archives of developmental biology.

[63]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[64]  Ken W. Y. Cho,et al.  Interaction of goosecoid and brachyury in Xenopus mesoderm patterning , 1997, Mechanisms of Development.

[65]  W. Müller.  Diacylglycerol-induced multihead formation in Hydra , 1989 .

[66]  E. Vieta,et al.  Molecular targets of lithium action , 2003, Acta Neuropsychiatrica.

[67]  T. Holstein,et al.  Stimulation of tentacle and bud formation by the neuropeptide head activator in Hydra magnipapillata. , 1997, Developmental biology.

[68]  F. McCormick,et al.  Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. , 2000, Journal of Biological Chemistry.

[69]  M. Peifer,et al.  Wnt signaling in oncogenesis and embryogenesis--a look outside the nucleus. , 2000, Science.

[70]  R. D. Campbell,et al.  Tissue dynamics of steady state growth in Hydra littoralis. I. Patterns of cell division. , 1967, Developmental biology.

[71]  H. Bode,et al.  Characterization of the head organizer in hydra. , 2002, Development.

[72]  C. N. David,et al.  Characterization of interstitial stem cells in hydra by cloning. , 1977, Developmental biology.

[73]  J. Woodgett,et al.  Wingless inactivates glycogen synthase kinase‐3 via an intracellular signalling pathway which involves a protein kinase C. , 1996, The EMBO journal.

[74]  G. E. Lesh-Laurie,et al.  Tentacle morphogenesis in hydra , 1972, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[75]  S. Hoffmeister.  Isolation and characterization of two new morphogenetically active peptides from Hydra vulgaris. , 1996, Development.

[76]  T. Holstein,et al.  Nerve cell differentiation in hydra requires two signals , 1986 .

[77]  F. Hauser,et al.  Expression and developmental regulation of the Hydra-RFamide and Hydra-LWamide preprohormone genes in Hydra: evidence for transient phases of head formation. , 1999, Developmental biology.

[78]  N. A. Stover,et al.  The level of expression of a protein kinase C gene may be an important component of the patterning process in Hydra , 1998, Development Genes and Evolution.

[79]  H. Bode,et al.  Selective disruption of gap junctional communication interferes with a patterning process in hydra. , 1987, Science.

[80]  R. D. Campbell.  Elimination by Hydra interstitial and nerve cells by means of colchicine. , 1976, Journal of cell science.

[81]  Patterning of the head in hydra as visualized by a monoclonal antibody, II. The initiation and localization of head structures in regenerating pieces of tissue. , 1988, Developmental biology.

[82]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. , 1974, Journal of cell science.

[83]  H. Bode,et al.  Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra. , 1997, Developmental biology.

[84]  T. Fujisawa,et al.  Genetic analysis of developmental mechanisms in hydra , 2005 .

[85]  T. Yao.  Studies on the Organizer Problem in Pelmatohydra Oligactis : I. The Induction Potency of the Implants and the Nature of the Induced Hydranth , 1945 .