Combining experiments and modelling to understand size regulation in Dictyostelium discoideum

Journal of the Royal Society Interface

Volumn 5, Issue SUPPL. 1, 2008, Pages

  Jang, Wonhee ^a   Gomer, Richard H ^b  

^a Dongguk University   (South Korea)

^b RICE UNIVERSITY   (United States)

Author keywords

Biological clocks; Dictyostelium; Size regulation

Indexed keywords

ADHESION; CELL ADHESION; COMPUTATIONAL METHODS; COMPUTER SIMULATION; EXPERIMENTS; FORECASTING; MECHANISMS;

ADHESION FORCES; CELL CELL ADHESION; CELL MOTILITY; CONCENTRATION (COMPOSITION); DICTYOSTELIUM DISCOIDEUM; DIFFUSION CALCULATIONS; GROUP SIZES; LOCAL CELL DENSITY; REGULATION MECHANISMS; SIMPLE SYSTEMS; UPPER LIMITS;

CELLS;

CELL PROTEIN; COUNTING FACTOR; PROTEIN CF45 1; PROTEIN CF50; PROTEIN CF60; PROTEIN COUNTIN; PROTOZOAL PROTEIN;

BODY SIZE; CALCULATION; CELL ADHESION; CELL COUNT; CELL DENSITY; CELL MOTILITY; CELL SECRETION; COMPUTER SIMULATION; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; DIFFUSION; EVOLUTION; NONHUMAN; PREDICTION; REGULATORY MECHANISM; REVIEW; SEQUENCE HOMOLOGY;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

EID: 46249085134     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2008.0067.focus     Document Type: Review

References (82)

1. Adames, N. R., Coukell, M. B. & Wu, L. 1994 Regulation of expression of the cyclic nucleotide phosphodiesterase gene in phosphodiesterase inhibitor-negative mutants of Dictyostelium discoideum. Biochem. Cell Biol. 72, 233-238.
2. Bergelson, J. M. & Hemler, M. E. 1995 Integrin-ligand binding. Do integrins use a 'MIDAS touch' to grasp an Asp? Curr. Biol. 5, 615-617. (doi:10.1016/S0960-9822 (95)00124-2)
3. Bohni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B. F., Bechingham, K. & Hafen, E. 1999 Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97, 865-875. (doi:10.1016/S0092-8674(00)80799-0)
4. Bonner, J. T. 2006 Why size matters: from bacteria to blue whales. Princeton, NJ: Princeton University Press.
5. Bosgraaf, L. & van Haastert, P. J. 2002 A model for cGMP signal transduction in Dictyostelium in perspective of 25 years of cGMP research. J. Muscle Res. Cell Motil. 23, 781-791. (doi:10.1023/A:1024431813040)
6. Bosgraaf, L. & van Haastert, P. J. 2006 The regulation of myosin II in Dictyostelium. Eur. J. Cell Biol. 85, 969-979. (doi:10.1016/j.ejcb.2006.04.004)
7. Brock, D. A. & Gomer, R. H. 1999 A cell-counting factor regulating structure size in Dictyostelium. Genes Dev. 13, 1960-1969. (doi:10.1101/gad.13.15.1960)
8. Brock, D. A., Buczynski, F., Spann, T. P., Wood, S. A., Cardelli, J. & Gomer, R. H. 1996 A Dictyostelium mutant with defective aggregate size determination. Development 122, 2569-2578.
9. Brock, D. A., Hatton, R. D., Giurgiutiu, D. V., Scott, B., Ammann, R. & Gomer, R. H. 2002 The different components of a multisubunit cell number-counting factor have both unique and overlapping functions. Development 129, 3657-3668.
10. Brock, D. A., Ehrenman, K., Ammann, R., Tang, Y. & Gomer, R. H. 2003a Two components of a secreted cell number-counting factor bind to cells and have opposing effects on cAMP signal transduction in Dictyostelium. J. Biol. Chem. 278, 52 262-52 272. (doi:10.1074/jbc.M309101200)
11. Brock, D. A., Hatton, R. D., Giurgiutiu, D. V., Scott, B., Jang, W., Ammann, R. & Gomer, R. H. 2003b CF45-1, a secreted protein which participates in Dictyostelium group size regulation. Eukaryot. Cell 2, 788-797. (doi:10.1128/EC.2.4.788-797.2003)
12. Brock, D. A., van Egmond, W. N., Shamoo, Y., Hatton, R. D. & Gomer, R. H. 2006 A 60-kilodalton protein component of the counting factor complex regulates group size in Dictyostelium discoideum. Eukaryot. Cell 5, 1532-1538. (doi:10.1128/EC.00169-06)
13. Brown, J. M. & Firtel, R. A. 2000 Just the right size: cell counting in Dictyostelium. Trends Genet. 16, 191-193. (doi:10.1016/S0168- 9525(00)01977-6)
14. Chae, S. C., Fuller, D. & Loomis, W. F. 2002 Altered cell-type proportioning in Dictyostelium lacking adenosine monophosphate deaminase. Dev. Biol. 241, 183-194. (doi:10.1006/dbio.2001.0491)
15. Chung, C. Y. & Firtel, R. A. 1999 PAKa, a putative PAK family member, is required for cytokinesis and the regulation of the cytoskeleton in Dictyostelium discoideum cells during chemotaxis. J. Cell Biol. 147, 559-576. (doi:10. 1083/jcb.147.3.559)
16. Chung, C. Y., Potikyan, G. & Firtel, R. A. 2001 Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol. Cell 7, 937-947. (doi:10.1016/S1097-2765(01)00247-7)
17. Clow, P. A. & McNally, J. G. 1999 In vivo observations of myosin II dynamics support a role in rear retraction. Mol. Biol. Cell 10, 1309-1323.
18. Conlon, I. & Raff, M. 1999 Size control in animal development. Cell 96, 235-244. (doi:10.1016/S0092-8674(00)80563-2)
19. Cox, D., Condeelis, J., Wessels, D., Soll, D., Kern, H. & Knecht, D. A. 1992 Targeted disruption of the ABP-120 gene leads to cells with altered motility. J. Cell Biol. 116, 943-955. (doi:10.1083/jcb.116.4.943)
20. Dallon, J., Jang, W. & Gomer, R. H. 2006 Mathematically modelling the effects of counting factor in Dictyostelium discoideum. Math. Med. Biol. 23, 45-62. (doi:10.1093/imammb/dqi016)
21. Deery, W. J. & Gomer, R. H. 1999 A putative receptor mediating cell-density sensing in Dictyostelium. J. Biol. Chem. 274, 34 476-34 482. (doi:10.1074/jbc.274.48.34476)
22. Deery, W. J., Gao, T., Ammann, R. & Gomer, R. H. 2002 A single cell density-sensing factor stimulates distinct signal transduction pathways through two different receptors. J. Biol. Chem. 277, 31 972-31 979. (doi:10.1074/jbc.M204539200)
23. de la Roche, M. A. & Côté, G. P. 2001 Regulation of Dictyostelium myosin I and II. Biochim. Biophys. Acta 1525, 245-261. (doi:10.1016/s0304-4165(01)00110-6)
24. Devreotes, P. 1989 Dictyostelium discoideum: a model system for cell-cell interactions in development. Science 245, 1054-1058. (doi:10.1126/science.2672337)
25. Faure, M., Podgorski, G. J., Franke, J. & Kessin, R. H. 1988 Disruption of Dictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase. Proc. Natl Acad. Sci. USA 85, 8076-8080. (doi:10.1073/pnas.85.21.8076)
26. Fero, M. L. et al. 1996 A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85, 733-744. (doi:10.1016/S0092- 8674(00)81239-8)
27. Firtel, R. A. 1995 Integration of signaling information in controlling cell-fate decisions in Dictyostelium. Genes Dev. 9, 1427-1444. (doi:10.1101/gad.9.12.1427)
28. Fukui, Y., de Hostos, E., Yumura, S., Kitanishi-Yumura, T. & Inou, S. 1999 Architectural dynamics of F-actin in eupodia suggests their role in invasive locomotion in Dictyostelium. Exp. Cell Res. 249, 33-45. (doi:10.1006/excr.1999.4445)
29. Gao, T., Ehrenman, K., Tang, L., Leippe, M., Brock, D. A. & Gomer, R. H. 2002 Cells respond to and bind countin, a component of a multisubunit cell number counting factor. J. Biol. Chem. 277, 32 596-32 605. (doi:10.1074/jbc. M203075200)
30. Gao, T., Knecht, D., Tang, L., Hatton, R. D. & Gomer, R. H. 2004 A cell number counting factor regulates Akt/protein kinase B to regulate Dictyostelium discoideum group size. Eukaryot. Cell 3, 1176-1184. (doi:10.1128/EC.3.5.1176-1184.2004)
31. Gao, T. et al. 2007 A cell number-counting factor regulates levels of a novel protein, SslA, as part of a group size regulation mechanism in Dictyostelium. Eukaryot. Cell 6, 1538-1551. (doi:10.1128/EC.00169- 07)
32. Garofalo, R. S. 2002 Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol. Metab. 13, 156-162. (doi:10.1016/S1043-2760(01)00548-3)
33. Garrod, D. R. & Ashworth, I. M. 1972 Effect of growth conditions on development of the cellular slime mould, Dictyostelium discoideum. J. Embryol. Exp. Morphol. 28, 463-479.
34. Gomer, R. H., Yuen, I. S. & Firtel, R. A. 1991 A secreted 80 X 10(3) Mr protein mediates sensing of cell density and the onset of development in Dictyostelium. Development 112, 269-278.
35. Gumbiner, B. M. 1996 Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357. (doi:10.1016/S0092-8674(00)81279-9)
36. Hohl, H. R. & Raper, K. B. 1964 Control of sorocarp size in the cellular slime mold Dictyostelium discoideum. Dev. Biol. 9, 137-153. (doi:10.1016/0012-1606(64)90018-1)
37. Jain, R. & Gomer, R. H. 1994 A developmentally regulated cell surface receptor for a density-sensing factor in Dictyostelium. J. Biol. Chem. 269, 9128-9136.
38. Jain, R., Yuen, I. S., Taphouse, C. R. & Gomer, R. H. 1992 A density-sensing factor controls development in Dictyostelium. Genes Dev. 6, 390-400. (doi:10.1101/gad.6.3.390)
39. Jang, W. & Gomer, R. H. 2005 Exposure of cells to a cell number-counting factor decreases the activity of glucose-6-phosphatase to decrease intracellular glucose levels in Dictyostelium discoideum. Eukaryot. Cell 4, 72-81. (doi:10. 1128/EC.4.1.72-81.2005)
40. Jang, W. & Gomer, R. H. 2006 A protein in crude cytosol regulates glucose-6-phosphatase activity in crude microsomes to regulate group size in Dictyostelium. J. Biol. Chem. 281, 16 377-16 383. (doi:10.1074/jbc.M509995200)
41. Jang, W., Chiem, B. & Gomer, R. H. 2002 A secreted cell number counting factor represses intracellular glucose levels to regulate group size in Dictyostelium. J. Biol. Chem. 277, 39 202-39 208. (doi:10.1074/jbc.M205635200)
42. Jin, T. & Hereld, D. 2006 Moving toward understanding eukaryotic chemotaxis. Eur. J. Cell Biol. 85, 905-913. (doi:10.1016/j.ejcb. 2006.04.008)
43. -) forms small fruiting bodies. Microbes Environ. 18, 223-226. (doi:10.1264/jsme2.18.223)
44. Kessin, R. H. 2001 Dictyostelium evolution, cell biology, and the development of multicellularity. In Developmental and cell biology series. New York, NY: Cambridge University Press.
45. Khosla, M., Spiegelman, G. B. & Weeks, G. 1996 Overexpression of an activated rasG gene during growth blocks the initiation of Dictyostelium development. Mol. Cell Biol. 16, 4156-4162.
46. Kiyokawa, H. et al. 1996 Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85, 721-732. (doi:10.1016/S0092-8674(00)81238-6)
47. Kopachik, W. 1982 Size regulation in Dictyostelium. J. Embryol. Exp. Morphol. 68, 23-35.
48. Loomis, W. F. 1975 Dictyostelium discoideum: a developmental system. New York, NY: Academic Press.
49. Mato, J. M., Krens, F. A., van Haastert, P. J. & Konijn, T. M. 1977 3′:5′-cyclic AMP-dependent 3′:5′-cyclic GMP accumulation in Dictyostelium discoideum. Proc. Natl Acad. Sci. USA 74, 2348-2351. (doi:10.1073/pnas.74.6.2348)
50. McPherron, A. & Lee, S. 1997 Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl Acad. Sci. USA 94, 12 457-12 461. (doi:10.1073/pnas.94.23.12457)
51. McPherron, A. C., Lawler, A. M. & Lee, S.-J. 1997 Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 8390. (doi:10.1038/387083a0)
52. Metcalf, D., Greenhalgh, C. J., Viney, E., Willson, T. A., Starr, R., Nicola, N. A., Hilton, D. J. & Alexander, W. S. 2000 Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 405, 1069-1073. (doi:10.1038/35016611)
53. Montagne, J., Stewart, M. J., Stocker, H., Hafen, E., Kozma, S. C. & Thomas, G. 1999 Drosophila S6 kinase: a regulator of cell size. Science 285, 2126-2129. (doi:10.1126/science. 285.5436.2126)
54. Moores, S., Sabry, J. & Spudich, J. 1996 Myosin dynamics in live Dictyostelium cells. Proc. Natl Acad. Sci. USA 93, 443-446. (doi:10.1073/pnas.93.1.443)
55. Nachmias, V. T., Fukui, Y. & Spudich, J. A. 1989 Chemoattractant- elicited translocation of myosin in motile Dictyostelium. Cell Motil. Cytoskel. 13, 158-169. (doi:10.1002/cm.970130304)
56. Nakayama, K., Ishida, N., Shirane, M., Inomata, A., Inoue, T., Shishido, N., Horii, I., Loh, D. Y. & Nakayama, K. 1996 Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85, 707-720. (doi:10.1016/S0092-8674(00) 81237-4)
57. Noegel, A. A. & Schleicher, M. 2000 The actin cytoskeleton of Dictyostelium: a story told by mutants. J. Cell Sci. 113(Pt 5), 759-766.
58. Ogihara, S., Carboni, J. & Condeelis, J. 1988 Electron microscopic localization of myosin II and ABP-120 in the cortical actin matrix of Dictyostelium amoebae using IgG-gold conjugates. Dev. Genet. 9, 505-520. (doi:10.1002/dvg.1020090427)
59. Okuwa, T., Katayama, T., Takano, A., Kodaira, K. & Yasukawa, H. 2001 Two cell-counting factors regulate the aggregate size of the cellular slime mold Dictyostelium discoideum. Dev. Growth Differ. 43, 735-744. (doi:10.1046/j.1440-169X.2001.00615.x)
60. Okuwa, T., Katayama, T., Takano, A. & Yasukawa, H. 2002 Identification of the homolog of cell-counting factor in the cellular slime mold Dictyostelium discoideum. J. Biochem. Mol. Biol. Biophys. 6, 351-355. (doi:10.1080/10258140 21000014001)
61. Oster, G. F., Murray, J. D. & Harris, A. K. 1983 Mechanical aspects of mesenchymal morphogenesis. J. Embryol. Exp. Morphol. 78, 83-125.
62. Parent, C. A. & Devreotes, P. N. 1999 A cell's sense of direction. Science 284, 765-770. (doi:10.1126/science.284. 5415.765)
63. Riedel, V., Gerisch, G., Muller, E. & Beug, H. 1973 Defective cyclic adenosine-3′,5′-phosphate-phosphodiesterase regulation in morphogenetic mutants of Dictyostelium discoideum. J. Mol. Biol. 74, 573-585. (doi:10.1016/0022-2836(73)90048-X)
64. Roisin-Bouffay, C., Jang, W., Caprette, D. R. & Gomer, R. H. 2000 A precise group size in Dictyostelium is generated by a cell-counting factor modulating cell-cell adhesion. Mol. Cell 6, 953-959. (doi:10.1016/S1097-2765(00)00093-9)
65. Roos, W., Nanjundiah, V., Malchow, D. & Gerisch, G. 1975 Amplification of cyclic-AMP signals in aggregating cells of Dictyostelium discoideum. FEBS Lett. 53, 139-142. (doi:10.1016/0014-5793(75)80005- 6)
66. Schaap, P. 1991 Intercellular interactions during Dictyostelium development. In Microbial cell-cell interactions (ed. M. Dworkin), pp. 147-178. Washington, DC: American Society of Microbiology.
67. Shaffer, B. M. 1957 Variability of behavior of aggregating cellular slime moulds. Quart. J. Microb. Sci. 98, 393-405.
68. Shaffer, B. M. 1975 Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mould Dictyostelium discoideum. Nature 255, 549-552. (doi:10.1038/255549a0)
69. Siu, C. H. 1990 Cell-cell adhesion molecules in Dictyostelium. Bioessays 12, 357-362. (doi:10.1002/bies.950120802)
70. Souza, G. M., Klein, C., Da Costa Maia, J. C. & Da Silva, A. M. 1994 Calcium uptake and gp80 messenger RNA destabilization follows cAMP receptor down regulation in Dictyostelium discoideum. Cell. Signal. 6, 883-895. (doi:10. 1016/0898-6568(94)90021-3)
71. Takeichi, M. 1993 Cadherins in cancer: implications for invasion and metastasis. Curr. Opin. Cell Biol. 5, 806-811. (doi:10.1016/0955-0674(93)90029-P)
72. Tang, L., Ammann, R., Gao, T. & Gomer, R. H. 2001 A cell number-counting factor regulates group size in Dictyostelium by differentially modulating cAMP-induced cAMP and cGMP pulse sizes. J. Biol. Chem. 276, 27 663-27 669. (doi:10.1074/jbc.M102205200)
73. Tang, L., Gao, T., McCollum, C., Jang, W., Vicker, M. G., Ammann, R. R. & Gomer, R. H. 2002 A cell number-counting factor regulates the cytoskeleton and cell motility in Dictyostelium. Proc. Natl Acad. Sci. USA 99, 1371-1376. (doi:10.1073/pnas.022516099)
74. Thadani, V., Pan, P. & Bonner, J. T. 1977 Complementary effects of ammonia and cAMP on aggregation territory size in the cellular slime mold Dictyostelium mucoroides. Exp. Cell Res. 108, 75-78. (doi:10.1016/s0014-4827(77)80011-6)
75. Turing, A. M. 1952 The chemical basis of morphogenesis. Phil. Trans. R. Soc. 237, 37-72. (doi:10.1098/rstb.1952.0012)
76. Van Haastert, P. J. & Veltman, D. M. 2007 Chemotaxis: navigating by multiple signaling pathways. Sci. STKE 2007, pe40. (doi:10.1126/stke.3962007pe40)
77. Varnum-Finney, B., Edwards, K. B., Voss, E. & Soll, D. R. 1987 Amebae of Dictyostelium discoideum respond to an increasing temporal gradient of the chemoattractant cAMP with a reduced frequency of turning: evidence for a temporal mechanism in ameboid chemotaxis. Cell Motil. Cytoskel. 8, 7-17. (doi:10.1002/cm.970080103)
78. Verkerke-van Wijk, I. & Schaap, P. 1997 cAMP, a signal for survival. In Dictyostelium - a model system for cell and developmental biology (eds Y. Maeda, K. Inouye & I. Takeuchi), pp. 145-162. Tokyo, Japan: Universal Academy Press.
79. Willard, S. S. & Devreotes, P. N. 2006 Signaling pathways mediating chemotaxis in the social amoeba, Dictyostelium discoideum. Eur. J. Cell Biol. 85, 897-904. (doi:10.1016/j.ejcb.2006.06.003)
80. Wurster, B., Schubiger, K., Wick, U. & Gerisch, G. 1977 Cyclic GMP in Dictyostelium discoideum. Oscillations and pulses in response to folic acid and cyclic AMP signals. FEBS Lett. 76, 141-144. (doi:10.1016/0014-5793(77) 80139-7)
81. Yuen, I. S. & Gomer, R. H. 1994 Cell density-sensing in Dictyostelium by means of the accumulation rate, diffusion coefficient and activity threshold of a protein secreted by starved cells. J. Theor. Biol. 167, 273-282. (doi:10.1006/jtbi.1994.1069)
82. Yuen, I. S., Jain, R., Bishop, J. D., Lindsey, D. F., Deery, W. J., Van Haastert, P. J. & Gomer, R. H. 1995 A density-sensing factor regulates signal transduction in Dictyostelium. J. Cell Biol. 129, 1251-1262. (doi:10.1083/jcb.129.5.1251)