Hydra, a versatile model to study the homeostatic and developmental functions of cell death

International Journal of Developmental Biology

Volumn 56, Issue 6-8, 2012, Pages 593-604

  Reiter, Silke ^a   Crescenzi, Marco ^b   Galliot, Brigitte ^a   Buzgariu, Wanda ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Apoptosis; Aposensor; Caspase inhibitors; DNA fragmentation; Flow cytometry

Indexed keywords

COLCHICINE; PROTEIN; SELF FEEDER 1; SF 1; UNCLASSIFIED DRUG; WORTMANNIN;

APOPTOSIS; ARTICLE; ASSAY; CELL DEATH; CELL LINE; CELL PROLIFERATION; CELL RENEWAL; CNIDARIA; DEVELOPMENT; DROSOPHILA; DRUG EXPOSURE; EPITHELIUM CELL; FLOW CYTOMETRY; FRESHWATER SPECIES; GENETIC CONSERVATION; GERM CELL; HEAT SENSITIVITY; HEAT SHOCK; HOMEOSTASIS; HUMAN; HYDRA; IMAGING; INTERSTITIAL CELL LINEAGE; MUTANT; NICK END LABELING; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; REGENERATION; SIGNAL TRANSDUCTION; SPERMATOGENESIS; STEM CELL; WOUND; XENOGRAFT;

ANIMALS; APOPTOSIS; DNA FRAGMENTATION; EPITHELIAL CELLS; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HYDRA; MODELS, ANIMAL; MULTIPOTENT STEM CELLS; OOGENESIS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; STEROIDOGENIC FACTOR 1;

HYDRA;

EID: 84864436446     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.123499sr     Document Type: Article

References (75)

1. ALEXANDROVA, O., SCHADE, M., BOTTGER, A., DAVID, C.N. (2005). Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Dev Biol 281: 91-101.
2. AUGUSTIN, R., BOSCH, T.C. (2011). Cnidarian immunity: a tale of two barriers. Adv Exp Med Biol 708: 1-16.
3. BARDET, P.L., KOLAHGAR, G., MYNETT, A., MIGUEL-ALIAGA, I., BRISCOE, J., MEIER, P., VINCENT, J.P. (2008). A fluorescent reporter of caspase activity for live imaging. Proc Natl Acad Sci USA 105: 13901-13905.
4. BARTKE, T., POHL, C., PYROWOLAKIS, G., JENTSCH, S. (2004). Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol Cell 14: 801-811.
5. BERGMANN, A., STELLER, H. (2010). Apoptosis, stem cells, and tissue regeneration. Sci Signal 3: re8.
6. BIBB, C., CAMPBELL, R.D. (1973). Cell affinity determining heterospecific graft intolerance in hydra. Tissue Cell 5: 199-208.
7. BOSCH, T.C. (1986). lmmunocompetence in Hydra: epithelial cells recognize self-nonself and react against it. J Exp Zool 238: 225-234.
8. BOSCH, T.C., DAVID, C.N. (1984). Growth regulation in Hydra: relationship between epithelial cell cycle length and growth rate. Dev Biol 104: 161-171.
9. BOTTGER, A., ALEXANDROVA, O. (2007). Programmed cell death in Hydra. Semin Cancer Biol 17: 134-146.
10. BRIEN, P., VAN DEN EECKHOUDT, J.P. (1953). [Budding and regeneration in hydra irradiated with x-rays]. C R Acad Sci, 237: 756-758.
11. BUZGARIU, W., CHERA, S., GALLIOT, B. (2008). Methods to investigate autophagy during starvation and regeneration in hydra. Methods Enzymol 451: 409-437.
12. CAMPBELL, R.D. (1976). Elimination by Hydra interstitial and nerve cells by means of colchicine. J Cell Sci 21: 1-13.
13. CHAPMAN, J.A., KIRKNESS, E.F., SIMAKOV, O., HAMPSON, S.E., MITROS, T., WEINMAIER, T., RATTEI, T., BALASUBRAMANIAN, P.G., BORMAN, J., BUSAM, D., et al. (2010). The dynamic genome of Hydra. Nature 464: 592-596.
14. CHERA, S., BUZGARIU, W., GHILA, L., GALLIOT, B. (2009a). Autophagy in Hydra: A response to starvation and stress in early animal evolution. Biochim Biophys Acta 1793: 1432-1443.
15. CHERA, S., GHILA, L., DOBRETZ, K., WENGER, Y., BAUER, C., BUZGARIU, W., MARTINOU, J.C., GALLIOT, B. (2009b). Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 17: 279-289.
16. CHERA, S., GHILA, L., WENGER, Y., GALLIOT, B. (2011). Injury-induced activation of the MAPK/CREB pathway triggers apoptosis-induced compensatory proliferation in hydra head regeneration. Dev Growth Differ 53: 186-201.
17. CIKALA, M., ALEXANDROVA, O., DAVID, C.N., PROSCHEL, M., STIENING, B., CRAMER, P., BOTTGER, A. (2004). The phosphatidylserine receptor from Hydra is a nuclear protein with potential Fe(II) dependent oxygenase activity. BMC Cell Biol 5: 26.
18. CIKALA, M., WILM, B., HOBMAYER, E., BOTTGER, A., DAVID, C.N. (1999). Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol 9: 959-962.
19. DARDING, M., MEIER, P. (2012). IAPs: Guardians of RIPK1. Cell Death Differ 19: 58-66.
20. DAVID, C., SCHMIDT, N., SCHADE, M., PAULY, B., ALEXANDROVA, O., BOTTGER, A. (2005). Hydra and the evolution of apoptosis. Integr Comp Biol 45: 631-638.
21. DEGTEREV, A., YUAN, J. (2008). Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9: 378-390.
22. DOMINGUES, C., RYOO, H.D. (2012). Drosophila BRUCE inhibits apoptosis through non-lysine ubiquitination of the IAP-antagonist REAPER. Cell Death Differ 19: 470-477.
23. DONTENWILL, M., PASCAL, G., PILETZ, J.E., CHEN, M., BALDWIN, J., RONDE, P., DUPUY, L., UROSEVIC, D., GRENEY, H., TAKEDA, K., BOUSQUET, P. (2003). IRAS, the human homologue of Nischarin, prolongs survival of transfected PC12 cells. Cell Death Differ 10: 933-935.
24. FEOKTISTOVA, M., GESERICK, P., KELLERT, B., DIMITROVA, D.P., LANGLAIS, C., HUPE, M., CAIN, K., MACFARLANE, M., HACKER, G., LEVERKUS, M. (2011). cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 43: 449-463.
25. FUCHS, Y., STELLER, H. (2011). Programmed cell death in animal development and disease. Cell 147: 742-758.
26. FUJISAWA, T., DAVID, C.N. (1984). Loss of differentiating nematocytes induced by regeneration and wound healing in Hydra. J Cell Sci 68: 243-255.
27. FULDA, S., PERVAIZ, S. (2010). Apoptosis signaling in cancer stem cells. Int J Biochem Cell Biol 42: 31-38.
28. GALLIOT, B., CHERA, S. (2010). The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol 20: 514-523.
29. GALLIOT, B., GHILA, L. (2010). Cell plasticity in homeostasis and regeneration. Mol Reprod Dev 77: 837-855.
30. GAUCHAT, D., ESCRIVA, H., MILJKOVIC-LICINA, M., CHERA, S., LANGLOIS, M.C., BEGUE, A., LAUDET, V., GALLIOT, B. (2004). The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev Biol 275: 104-123.
31. HOLSTEIN, T.W., HOBMAYER, E., DAVID, C.N. (1991). Pattern of epithelial cell cycling in hydra. Dev Biol 148: 602-611.
32. HONEGGER, T.G., ZURRER, D., TARDENT, P. (1989). Oogenesis in Hydra carnea: A new model based on light and electron microscopic analyses of oocyte and nurse cell differentiation. Tissue Cell 21: 381-393.
33. KALOULIS, K., CHERA, S., HASSEL, M., GAUCHAT, D., GALLIOT, B. (2004). Reactivation of developmental programs: the cAMP-response element-binding protein pathway is involved in hydra head regeneration. Proc Natl Acad Sci USA 101: 2363-2368.
34. KANOME, T., ITOH, N., ISHIKAWA, F., MORI, K., KIM-KANEYAMA, J.R., NOSE, K., SHIBANUMA, M. (2007). Characterization of Jumping translocation breakpoint (JTB) gene product isolated as a TGF-beta1-inducible clone involved in regulation of mitochondrial function, cell growth and cell death. Oncogene 26: 5991-6001.
35. KUZNETSOV, S., LYANGUZOWA, M., BOSCH, T.C. (2001). Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104: 25-31.
36. KUZNETSOV, S.G., ANTON-ERXLEBEN, F., BOSCH, T.C. (2002). Epithelial interactions in Hydra: apoptosis in interspecies grafts is induced by detachment from the extracellular matrix. J Exp Biol 205: 3809-3817.
37. LANGE, C., HEMMRICH, G., KLOSTERMEIER, U.C., LOPEZ-QUINTERO, J.A., MILLER, D.J., RAHN, T., WEISS, Y., BOSCH, T.C., ROSENSTIEL, P. (2011). Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol Biol Evol 28: 1687-1702.
38. LASI, M., DAVID, C.N., BOTTGER, A. (2010a). Apoptosis in pre-Bilaterians: Hydra as a model. Apoptosis 15: 269-278.
39. LASI, M., PAULY, B., SCHMIDT, N., CIKALA, M., STIENING, B., KASBAUER, T., ZENNER, G., POPP, T., WAGNER, A., KNAPP, R.T., HUBER, A.H., GRUNERT, M., SODING, J., DAVID, C.N., BOTTGER, A. (2010b). The molecular cell death machinery in the simple cnidarian Hydra includes an expanded caspase family and pro-and anti-apoptotic Bcl-2 proteins. Cell Res 20: 812-825.
40. LIN, Y., DEVIN, A., COOK, A., KEANE, M.M., KELLIHER, M., LIPKOWITZ, S., LIU, Z.G. (2000). The death domain kinase RIP is essential for TRAIL (Apo2L)-induced activation of IkappaB kinase and c-Jun N-terminal kinase. Mol Cell Biol 20: 6638-6645.
41. LINDGENS, D., HOLSTEIN, T.W., TECHNAU, U. (2004). Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. Development 131: 191-201.
42. LITTLEFIELD, C.L. (1991). Cell lineages in Hydra: isolation and characterization of an interstitial stem cell restricted to egg production in Hydra oligactis. Dev Biol 143: 378-388.
43. LUTHRINGER, B., ISBERT, S., MULLER, W.E., ZILBERBERG, C., THAKUR, N.L., WORHEIDE, G., STAUBER, R.H., KELVE, M., WIENS, M. (2011). Poriferan survivin exhibits a conserved regulatory role in the interconnected pathways of cell cycle and apoptosis. Cell Death Differ 18: 201-213.
44. MARCUM, B.A., FUJISAWA, T., SUGIYAMA, T. (1980). A mutant hydra strain (sf-1) containing temperature-sensitive interstitial cells, in: TARDENT, P., TARDENT, R. (Eds.), Developmental and Cellular Biology of Coelenterates. Elsevier/North Holland, Amsterdam, pp. 429-434.
45. MARTINEZ, D., BRIDGE, D. (2012). Hydra, the everlasting embryo, confronts aging. Int J Dev Biol 56: 479-487.
46. MARTINOU, J.C., YOULE, R.J. (2011). Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21: 92-101.
47. MCDONALD, E.R., 3RD, EL-DEIRY, W.S. (2004). Suppression of caspase-8-and-10-associated RING proteins results in sensitization to death ligands and inhibition of tumor cell growth. Proc Natl Acad Sci USA 101: 6170-6175.
48. MILJKOVIC-LICINA, M., CHERA, S., GHILA, L., GALLIOT, B. (2007). Head regeneration in wild-type hydra requires de novo neurogenesis. Development 134: 1191-1201.
49. MILLER, M.A., TECHNAU, U., SMITH, K.M., STEELE, R.E. (2000). Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 224: 326-338.
50. MIURA, M. (2011). Active participation of cell death in development and organismal homeostasis. Dev Growth Differ 53: 125-136.
51. MULLER-TAUBENBERGER, A., VOS, M.J., BOTTGER, A., LASI, M., LAI, F.P., FISCHER, M., ROTTNER, K. (2006). Monomeric red fluorescent protein variants used for imaging studies in different species. Eur J Cell Biol 85: 1119-1129.
52. NISHIMAYA-FUJISAWA, C. (2012). Germline stem cells and sex determination in Hydra. Int J Dev Biol 56: 499-508.
53. O'CONNOR, W., JR., HARTON, J.A., ZHU, X., LINHOFF, M.W., TING, J.P. (2003). Cutting edge: CIAS1/cryopyrin/PYPAF1/NALP3/CATERPILLER 1.1 is an inducible inflammatory mediator with NF-kappa B suppressive properties. J Immunol 171: 6329-6333.
54. ORMEROD, M.G. (2000). Flow cytometry: a practical approach, 3rd ed. Oxford University Press, Oxford.
55. OTTO, J.J., CAMPBELL, R.D. (1977). Tissue economics of hydra: regulation of cell cycle, animal size and development by controlled feeding rates. J Cell Sci 28: 117-132.
56. PACHURA, S., CAMBON, J.P., BLAISE, C., VASSEUR, P. (2005). 4-nonylphenol-induced toxicity and apoptosis in Hydra attenuata. Environ Toxicol Chem, 24: 3085-3091.
57. PODRABSKY, J.E., KRUMSCHNABEL, G. (2010). Cell death beyond worms, flies and humans: Unusual model systems for cell death research. Apoptosis 15: 243-248.
58. QIU, X.B., MARKANT, S.L., YUAN, J., GOLDBERG, A.L. (2004). Nrdp1-mediated degradation of the gigantic IAP, BRUCE, is a novel pathway for triggering apoptosis. EMBO J 23: 800-810.
59. RIBEIRO, P.S., KURANAGA, E., TENEV, T., LEULIER, F., MIURA, M., MEIER, P. (2007). DIAP2 functions as a mechanism-based regulator of drICE that contributes to the caspase activity threshold in living cells. J Cell Biol 179: 1467-1480.
60. SHIMIZU, H. (2012). Transplantation analysis of developmental mechanisms in Hydra. Int J Dev Biol 56: 463-472.
61. SHIMIZU, S., KONISHI, A., NISHIDA, Y., MIZUTA, T., NISHINA, H., YAMAMOTO, A., TSUJIMOTO, Y. (2010). Involvement of JNK in the regulation of autophagic cell death. Oncogene 29: 2070-2082.
62. SRINIVASULA, S.M., ASHWELL, J.D. (2008). IAPs: what's in a name? Mol Cell 30: 123-135.
63. SRIVASTAVA, M., SIMAKOV, O., CHAPMAN, J., FAHEY, B., GAUTHIER, M.E., MITROS, T., RICHARDS, G.S., CONACO, C., DACRE, M., HELLSTEN, U. et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726.
64. STRELIN, G.S. (1929). Röntgenologische Untersuchungen an Hydren. II. Die histologischen Verianderungen im Korperbau von Pelmatohydra oligactis unter der Wirkung der Röntgenstrahlen und ihre Bedeutung für die Regeneration und Vermehrung. Roux's Arch Entw Mech Org 115: 26-51.
65. SUGIYAMA, T., FUJISAWA, T. (1978). Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. J Cell Sci 29: 35-52.
66. TECHNAU, U., MILLER, M.A., BRIDGE, D., STEELE, R.E. (2003). Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev Biol 260: 191-206.
67. TENEV, T., BIANCHI, K., DARDING, M., BROEMER, M., LANGLAIS, C., WALLBERG, F., ZACHARIOU, A., LOPEZ, J., MACFARLANE, M., CAIN, K., MEIER, P. (2011). The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43: 432-448.
68. TERADA, H., SUGIYAMA, T., SHIGENAKA, Y. (1988). Genetic analysis of developmental mechanisms in hydra. XVIII. Mechanism for elimination of the interstitial cell lineage in the mutant strain Sf-1. Dev Biol 126: 263-269.
69. VAN VLIERBERGHE, P., MEIJERINK, J.P., LEE, C., FERRANDO, A.A., LOOK, A.T., VAN WERING, E.R., BEVERLOO, H.B., ASTER, J.C., PIETERS, R. (2006). A new recurrent 9q34 duplication in pediatric T-cell acute lymphoblastic leukemia. Leukemia 20: 1245-1253.
70. VERNOOY, S.Y., CHOW, V., SU, J., VERBRUGGHE, K., YANG, J., COLE, S., OLSON, M.R., HAY, B.A. (2002). Drosophila Bruce can potently suppress Rpr-and Grim-dependent but not Hid-dependent cell death. Curr Biol 12: 1164-1168.
71. WILKINSON, J.C., RICHTER, B.W., WILKINSON, A.S., BURSTEIN, E., RUMBLE, J.M., BALLIU, B., DUCKETT, C.S. (2004). VIAF, a conserved inhibitor of apoptosis (IAP)-interacting factor that modulates caspase activation. J Biol Chem 279: 51091-51099.
72. YAROSS, M.S., BODE, H.R. (1978). Regulation of interstitial cell differentiation in Hydra attenuata. V. Inability of regenerating head to support nematocyte differentiation. J Cell Sci 34: 39-52.
73. YI, C.H., YUAN, J. (2009). The Jekyll and Hyde functions of caspases. Dev Cell 16: 21-34.
74. ZIHLER, J. (1972). Zur Gametogenese und Befructungsbiologie von Hydra. Wilhelm Rouxs Arch. Entwick Mech Org 169: 239-267.
75. ZOU, H., LI, Y., LIU, X., WANG, X. (1999). An APAF-1. cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274: 11549-11556.