Summary
The role of the cellular environment on hydra stem cell proliferation and differentiation was investigated by introduction of interstitial cells into host tissue of defined cellular composition. In epithelial tissue lacking all non-epithelial cells the interstitial cell population did not grow but differentiated into nerve cells and nematocytes. In host tissue with progressively increased numbers of nerve cells growth of the interstitial cell population was positively correlated to the nerve cell density. In agreement with previous observations (Bode et al. 1976), growth of the interstitial cell population was also found to be negatively correlated to the level of interstitial cells present. The strong correlation between the growth of the interstitial cell population and the presence of interstitial cells and nerve cells implies that interstitial cell proliferation is controlled by a feedback signal from interstitial cells and their derivatives. Our results suggest that the cellular environment of interstitial cells provides cues which are instrumental in stem cell decision making.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bartocci A, Mastrogiannis DS, Mighorati G, Stockert RJ, Wolkoff AW, Stanley ER (1987) Macrophages specifically regulate the concentration of their own growth factor in the circulation. Proc Natl Acad Sci USA 84:6179–6183
Bode HR, Flick KM, Smith GS (1976) Regulation of interstitial cell differentiation in Hydra attenuata: Relationship between epithelial cell cycle length and growth rate. J Cell Sci 20:29–46
Bosch TCG, David CN (1984) Growth regulation in Hydra: Relationship between epithelial cell cycle length and growth rate. Dev Biol 104:161–171
Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191
Campbell RD (1976) Elimination of Hydra interstitial and nerve cells by means of colchicine. J Cell Sci 21:1–13
David CN (1973) A quantitative method for maceration of Hydra tissue. Roux Arch Entw Mech Org 171:259–268
David CN, Gierer A (1974) Cell cycle Kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation J Cell Sci 16:359–375
David CN, Murphy S (1977) Characterization of interstitial stem cells in hydra by cloning. Dev Biol 58:372–383
David CN, MacWilliams H (1978) Regulation of the self-renewal capacity in Hydra stem cell clones. Proc Natl Acad Sci USA 75:886–890
David CN, Bosch TCG, Hobmeyer E, Holstein T, Schmidt T (1987) Interstitial stem cells in hydra. In: Loomis WF (ed) Genetic regulation of development. Alan Liss, New York, pp 389–408
Fujisawa T, David CN (1984) Loss of differentiating nematocytes induced by regeneration and wound healing in Hydra. J Cell Sci 68:243–255
Fujisawa T, David CN, Bosch TCG (1990) Transplantation stimulates interstitial cell migration in hydra. Dev Biol 138:509–512
Gordon MY, Dowding CR, Riley GP, Goldman JM, Graves MF (1987) Altered adhesive interactions with marrow stroma of haematopoietic progenitor cells in chronic myeloid leukaemia. Nature 328:342–344
Graham GJ, Wright EG, Hewick R, Wolpe SD, Wilkie NM, Donaldson D, Lorimore S, Pragnell IB (1990) Identification and characterization of an inhibitor of hemopoietic stem cell proliferation. Nature 344:442–444
Hall PA, Watt FM (1989) Stem cells: The generation and maintenance of cellular diversity. Development 106:619–633
Harlow E, Lane D (1988) Antibodies. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Heimfeld S, Bode HR (1985) Growth regulation of the interstitial cell population in hydra. I. Evidence for global control by nerve cells in the head. Dev Biol 110:297–307
Heimfeld S, Bode HR (1986) Growth regulation of the interstitial cell population in hydra. 111. Interstitial cell density does not control stem cell proliferation. Dev Biol 116:51–58
Hobmeyer E, Holstein T, David CN (1990) Tentacle morphogenesis in hydra. II. Formation of a complex between a sensory nerve cell and a battery cell. Development 109:897–904
Itoh K, Tezuka H, Sakoda H, Konno M, Nagata K, Uchiyama T, Uchino H, Mori KJ (1989) Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow. Exp Hematol 17:145–153
Johnson A, Dorshkind K (1986) Stromal cells in myeloid and lymphoid long-term bone marrow cultures can support multiple hemopoietic lineages and modulate their production of hemopoietic growth factors. Blood 68:1348
Lajtha LG (1979) Stem cell concepts. Differentiation 14:1–11
Littlefield LC (1986) Sex determination in hydra: control by a subpopulation of interstitial cells in Hydra oligactis males. Dev Biol 117:428–434
Lord BI, Dexter TM (1988) Stem cells. J Cell Sci (Suppl) 10:1–283
Marcum BA, Campbell RD (1983) Eliminating all non-epithelial cells using colchicine. In: Lenhoff HM (ed) Hydra: Research methods. Plenum Press, New York, pp 281–286
Marcum BA, Sugiyama T, Fujisawa T (1980) A mutant 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
Metcalf D (1989) The molecular control of cell division, differentiation commitment and maturation in hemopoietic cells. Nature 329:27–30
Okamoto T, Anthony K, Mintz B (1985) Abnormal development of genetically normal fetal hematopoietic stem cells in steel mutant mouse fetuses. Dev Biol 109:251–254
Plickert G, Kroiher M (1988) Proliferation kinetics and cell lineages can be studied in whole mounts and macerates by means of BrdU/anti-BrdU technique. Development 103:791–794
Rubin DI, Bode HR (1982) Nematocyte develoment in Hydra attenuata is dependent on both the interstitial cells and the epithelial cells. Dev Biol 90: 306–314
Sproull F, David CN (1979) Stem cell growth and differentiation in Hydra attenuata. II. Regulation of nerve and nematocyte differentiation in multiclone aggregates. J Cell Sci 38:155–169
Sugiyama T, Sugimoto N (1985) Genetic analysis of developmental mechanisms in hydra. XI. Mechanisms of sex reversal by heterosexual parabiosis. Dev Biol 110:413–421
Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in hydra. I. Sexual reproduction of Hydra magnipapillata and isolation of mutants. Dev Growth Diff 19:187–200
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
Wanek N, Marcum BA, Campbell RD (1980) Histological structure of epithelial hydra and evidence for the complete absence of interstitial cells and nerve cells. J Exp Zool 212:1–11
Whetton AD, Dexter TM (1986) Haemopoietic growth factors. TIBS 11:207–211
Yaross MS, Bode HR (1978) Regulation of interstitial cell differentiation in Hydra attenuata. III. Effects of i-cell and nerve cell densities. J Cell Sci 34:1–25
Author information
Authors and Affiliations
Additional information
Offprint requests to: T.C.G. Bosch
Rights and permissions
About this article
Cite this article
Bosch, T.C.G., Rollbühler, R., Scheider, B. et al. Role of the cellular environment in interstitial stem cell proliferation in Hydra . Roux's Arch Dev Biol 200, 269–276 (1991). https://doi.org/10.1007/BF00241296
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00241296