Injury-induced activation of the MAPK/CREB pathway triggers apoptosis-induced compensatory proliferation in hydra head regeneration

Development Growth and Differentiation

Volumn 53, Issue 2, 2011, Pages 186-201

  Chera, Simona ^a   Ghila, Luiza ^a   Wenger, Yvan ^a   Galliot, Brigitte ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Apoptosis induced compensatory proliferation; CREB binding protein; Hydra regeneration; Injury induced apoptosis; MAPK ERK CREB pathway; Ribosomal S6 kinase

Indexed keywords

BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; S6 KINASE; WNT3 PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL PROLIFERATION; ENZYME ACTIVATION; GENETIC CONSERVATION; HEAD; HYDRA; INJURY; NONHUMAN; NUCLEOTIDE SEQUENCE; TISSUE REGENERATION;

ANIMALS; APOPTOSIS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HYDRA; MITOGEN-ACTIVATED PROTEIN KINASES; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION;

BILATERIA; HYDRA;

EID: 79951826319     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2011.01250.x     Document Type: Article

References (79)

1. Arvizu, F., Aguilera, A. & Salgado, L. M. 2006. Activities of the protein kinases STK, PI3K, MEK, and ERK are required for the development of the head organizer in Hydra magnipapillata. Differentiation 74, 305-312.
2. Bergantinos, C., Corominas, M. & Serras, F. 2010a. Cell death-induced regeneration in wing imaginal discs requires JNK signalling. Development 137, 1169-1179.
3. Bergantinos, C., Vilana, X., Corominas, M. & Serras, F. 2010b. Imaginal discs: renaissance of a model for regenerative biology. Bioessays 32, 207-217.
4. Bergmann, A. & Steller, H. 2010. Apoptosis, stem cells, and tissue regeneration. Sci. Signal 3. re8.
5. Bhoumik, A., Huang, T. G., Ivanov, V., Gangi, L., Qiao, R. F., Woo, S. L., Chen, S. H. & Ronai, Z. 2002. An ATF2-derived peptide sensitizes melanomas to apoptosis and inhibits their growth and metastasis. J. Clin. Invest. 110, 643-650.
6. Bosch, M., Serras, F., Martin-Blanco, E. & Baguna, J. 2005. JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev. Biol. 280, 73-86.
7. Bosch, T. C. 2007. Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. Dev. Biol. 303, 421-433.
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. Bridge, D., Theofiles, A. G., Holler, R. L., Marcinkevicius, E., Steele, R. E. & Martinez, D. E. 2010. FoxO and stress responses in the cnidarian Hydra vulgaris. PLoS ONE 5, e11686.
10. Browne, E. N. 1909. The production of new hydranths in hydra by the insertion of small grafts. J. Exp. Zool. 7, 1-37.
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. Chambon, J. P., Nakayama, A., Takamura, K., McDougall, A. & Satoh, N. 2007. ERK- and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles. Development 134, 1203-1219.
14. Chen, B. P., Liang, G., Whelan, J. & Hai, T. 1994. ATF3 and ATF3 delta Zip. Transcriptional repression versus activation by alternatively spliced isoforms. J. Biol. Chem. 269, 15819-15826.
15. 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.
16. Chera, S., de Rosa, R., Miljkovic-Licina, M., Dobretz, K., Ghila, L., Kaloulis, K. & Galliot, B. 2006. Silencing of the hydra serine protease inhibitor Kazal1 gene mimics the human SPINK1 pancreatic phenotype. J. Cell Sci. 119, 846-857.
17. 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.
18. Chera, S., Kaloulis, K. & Galliot, B. 2007. The cAMP response element binding protein (CREB) as an integrative HUB selector in metazoans: clues from the hydra model system. Biosystems 87, 191-203.
19. 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.
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. Fan, Y. & Bergmann, A. 2008. Distinct mechanisms of apoptosis-induced compensatory proliferation in proliferating and differentiating tissues in the Drosophila eye. Dev. Cell. 14, 399-410.
22. Fujisawa, T. & David, C. N. 1984. Loss of differentiating nematocytes induced by regeneration and wound healing in Hydra. J. Cell Sci. 68, 243-255.
23. Galliot, B. & Chera, S. 2010. The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol. 20, 514-523.
24. Galliot, B. & Ghila, L. 2010. Cell plasticity in homeostasis and regeneration. Mol. Reprod. Dev. 77, 837-855. in press.
25. Galliot, B., Miljkovic-Licina, M., de Rosa, R. & Chera, S. 2006. Hydra, a niche for cell and developmental plasticity. Semin. Cell Dev. Biol. 17, 492-502.
26. Galliot, B. & Schmid, V. 2002. Cnidarians as a model system for understanding evolution and regeneration. Int. J. Dev. Biol. 46, 39-48.
27. Galliot, B., Welschof, M., Schuckert, O., Hoffmeister, S. & Schaller, H. C. 1995. The cAMP response element binding protein is involved in hydra regeneration. Development 121, 1205-1216.
28. 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.
29. Gauchat, D., Kreger, S., Holstein, T. & Galliot, B. 1998. prdl-a, a gene marker for hydra apical differentiation related to triploblastic paired-like head-specific genes. Development 125, 1637-1645.
30. Gierer, A., Berking, S., Bode, H., David, C. N., Flick, K., Hansmann, G., Schaller, H. & Trenkner, E. 1972. Regeneration of hydra from reaggregated cells. Nat. New Biol. 239, 98-101.
31. Gumienny, T. L., Lambie, E., Hartwieg, E., Horvitz, H. R. & Hengartner, M. O. 1999. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126, 1011-1022.
32. Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbacher, U. & Holstein, T. W. 2000. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407, 186-189.
33. Holstein, T. W., Hobmayer, E. & Technau, U. 2003. Cnidarians: an evolutionarily conserved model system for regeneration? Dev. Dyn. 226, 257-267.
34. 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.
35. Hua, B., Tamamori-Adachi, M., Luo, Y., Tamura, K., Morioka, M., Fukuda, M., Tanaka, Y. & Kitajima, S. 2006. A splice variant of stress response gene ATF3 counteracts NF-kappaB-dependent anti-apoptosis through inhibiting recruitment of CREB-binding protein/p300 coactivator. J. Biol. Chem. 281, 1620-1629.
36. Huh, J. R., Guo, M. & Hay, B. A. 2004. Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14, 1262-1266.
37. Hwang, J. S., Kobayashi, C., Agata, K., Ikeo, K. & Gojobori, T. 2004. Detection of apoptosis during planarian regeneration by the expression of apoptosis-related genes and TUNEL assay. Gene 333, 15-25.
38. Kaloulis, K. 2000. Molecular basis of morphogenetic events in hydra: study of the creb and hedgehog pathways during budding and regeneration. In: PhD dissertation. Department of Zoology and Animal Biologypp. 35-37, University of Geneva, Geneva.
39. 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. U S A. 101, 2363-2368.
40. Kondo, S. 1988. Altruistic cell suicide in relation to radiation hormesis. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 53, 95-102.
41. Kuranaga, E., Kanuka, H., Igaki, T., Sawamoto, K., Ichijo, H., Okano, H. & Miura, M. 2002. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 4, 705-710.
42. Kuranaga, E. & Miura, M. 2002. Molecular genetic control of caspases and JNK-mediated neural cell death. Arch. Histol. Cytol. 65, 291-300.
43. Kuranaga, E. & Miura, M. 2007. Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol. 17, 135-144.
44. Kuznetsov, S., Lyanguzowa, M. & Bosch, T. C. 2001. Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104, 25-31.
45. 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.
46. Lasi, M., David, C. N. & Bottger, A. 2010a. Apoptosis in pre-Bilaterians: Hydra as a model. Apoptosis 15, 269-278.
47. Lasi, M., Pauly, B., Schmidt, N., Cikala, M., Stiening, B., Kasbauer, T., Zenner, G., Popp, T., Wagner, A, Knapp, RT, Huber, AH, Grunert, M, Soding, J, David, CN & 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.
48. Lengfeld, T., Watanabe, H., Simakov, O., Lindgens, D., Gee, L., Law, L., Schmidt, H. A., Ozbek, S. et al. 2009. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev. Biol. 330, 186-199.
49. Li, F., Huang, Q., Chen, J., Peng, Y., Roop, D. R., Bedford, J. S. & Li, C. Y. 2010. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci. Signal 3, ra13.
50. Lin, A. 2003. Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 25, 17-24.
51. MacWilliams, H. K. 1983. Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. Dev. Biol. 96, 239-257.
52. Manuel, G. C., Reynoso, R., Gee, L., Salgado, L. M. & Bode, H. R. 2006. PI3K and ERK 1-2 regulate early stages during head regeneration in hydra. Dev. Growth Differ. 48, 129-138.
53. Martinez, D. E., Dirksen, M. L., Bode, P. M., Jamrich, M., Steele, R. E. & Bode, H. R. 1997. Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra. Dev. Biol. 192, 523-536.
54. Mayr, B. & Montminy, M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609.
55. 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.
56. Moreno, E., Yan, M. & Basler, K. 2002. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 12, 1263-1268.
57. Noda, K. 1971. Reconstitution of dissociated cells of hydra. Zool. Mag. 80, 99-101.
58. Otto, J. J. & Campbell, R. D. 1977a. Budding in Hydra attenuata: bud stages and fate map. J. Exp. Zool. 200, 417-428.
59. Otto, J. J. & Campbell, R. D. 1977b. Tissue economics of hydra: regulation of cell cycle, animal size and development by controlled feeding rates. J. Cell Sci. 28, 117-132.
60. Pellettieri, J., Fitzgerald, P., Watanabe, S., Mancuso, J., Green, D. R. & Sanchez Alvarado, A. 2010. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 338, 76-85.
61. Perez-Garijo, A., Martin, F. A. & Morata, G. 2004. Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131, 5591-5598.
62. Perez-Garijo, A., Shlevkov, E. & Morata, G. 2009. The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc. Development 136, 1169-1177.
63. Philipp, I., Holstein, T. W. & Hobmayer, B. 2005. HvJNK, a Hydra member of the c-Jun NH(2)-terminal kinase gene family, is expressed during nematocyte differentiation. Gene Expr. Patterns 5, 397-402.
64. Rentzsch, F., Guder, C., Vocke, D., Hobmayer, B. & Holstein, T. W. 2007. An ancient chordin-like gene in organizer formation of Hydra. Proc. Natl Acad. Sci. U S A. 104, 3249-3254.
65. Ryoo, H. D., Gorenc, T. & Steller, H. 2004. Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell. 7, 491-501.
66. Shimizu, H., Zhang, X., Zhang, J., Leontovich, A., Fei, K., Yan, L. & Sarras, M. P. Jr 2002. Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 129, 1521-1532.
67. Smith- Bolton, R. K., Worley, M. I., Kanda, H. & Hariharan, I. K. 2009. Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev. Cell. 16, 797-809.
68. Sohn, S. J., Lewis, G. M. & Winoto, A. 2008. Non-redundant function of the MEK5-ERK5 pathway in thymocyte apoptosis. EMBO J. 27, 1896-1906.
69. Steele, R. E. 2002. Developmental signaling in Hydra: what does it take to build a "simple" animal? Dev. Biol. 248, 199-219.
70. Technau, U. & Bode, H. R. 1999. HyBra1, a Brachyury homologue, acts during head formation in Hydra. Development 126, 999-1010.
71. Technau, U., Cramer Von Laue, C., Rentzsch, F., Luft, S., Hobmayer, B., Bode, H. R. & Holstein, T. W. 2000. Parameters of self-organization in hydra aggregates. Proc. Natl Acad. Sci. U S A. 97, 12127-12131.
72. 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.
73. 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.
74. Trembley, A.. 1744. Mémoires pour servir à l'histoire d'un genre de polypes d'eau douce, à bras en forme de cornes. Verbeck, Leiden. 334 p.
75. Tseng, A. S., Adams, D. S., Qiu, D., Koustubhan, P. & Levin, M. 2007. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev. Biol. 301, 62-69.
76. Vlaskalin, T., Wong, C. J. & Tsilfidis, C. 2004. Growth and apoptosis during larval forelimb development and adult forelimb regeneration in the newt (Notophthalmus viridescens). Dev. Genes. Evol. 214, 423-431.
77. Wang, L., Dai, W. & Lu, L. 2007. Stress-induced c-Jun activation mediated by Polo-like kinase 3 in corneal epithelial cells. J. Biol. Chem. 282, 32121-32127.
78. Warner, S. J., Yashiro, H. & Longmore, G. D. 2010. The Cdc42/Par6/aPKC Polarity Complex Regulates Apoptosis-Induced Compensatory Proliferation in Epithelia. Curr. Biol. 20, 677-686.
79. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. & Greenberg, M. E. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.