Cell death, survival and proliferation in Tetrahymena thermophila. Effects of insulin, sodium nitroprusside, 8-bromo cyclic GMP, N(G)-methyl-L-arginine and methylene blue

Cell Biology International

Volumn 20, Issue 10, 1996, Pages 653-666

  Christensen, Søren T ^a,b   Kemp, Kåre ^a   Quie, Helene ^a   Rasmussen, Leif ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell proliferation; Cell survival; Cyclic GMP; Insulin; Nitric oxide; Sodium nitroprusside; Tetrahymena thermophila

Indexed keywords

8 BROMO CYCLIC GMP; ARGININE; HEMIN; INSULIN; METHYLENE BLUE; N(G) METHYLARGININE; NITROPRUSSIDE SODIUM; PROTOPORPHYRIN;

ARTICLE; CELL DEATH; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; NONHUMAN; TETRAHYMENA THERMOPHILA;

BOVINAE; CILIOPHORA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 0030272157     PISSN: 10656995     EISSN: None     Source Type: Journal    
DOI: 10.1006/cbir.1996.0087     Document Type: Article

References (77)

1. AMEISEN JC, IDZIOREK T, BILLAUT-MULOT O, LOYENS M, TISSIER J-P, POTENTIER A, OUAISSI A, 1995. Apoptosis in a unicellular eukaryote (Trypanosoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Cell Death Diff 2: 285-300.
2. BERELOWITZ M, LEROITH D, VON SCHENK H, et al., 1982. Somatostatin-like immunoactivity and biological activity is present in Tetrahymena pyriformis, a ciliated protozoan. Endocrinology 110: 1939-1944.
3. 2+ and cyclic nucleotides. Adv Sec Mess Phosph Res 23: 227-273.
4. CHRISTENSEN ST, 1993. Insulin rescues the unicellular eukaryote Tetrahymena from dying in a complete, synthetic medium. Cell Biol Int 17: 833-838.
5. CHRISTENSEN ST, KRISTIANSEN K, CHEMNITZ J, 1995a. Staurosporine induced death in Tetrahymena thermophila. J Euk Microbiol Abstracts 43: 25A.
6. CHRISTENSEN ST, QUIE H, KEMP K, RASMUSSEN L, 1996. Insulin produces a biphasic response in Tetrahymena thermophila by stimulating cell survival and activating cell proliferation in two separate concentration intervals. Cell Biol Int (in press).
7. CHRISTENSEN ST, RASMUSSEN L, 1992. Evidence for growth factors which control cell multiplication in Tetrahymena thermophila. Acta Protozool 31: 215-219.
8. CHRISTENSEN ST, SCHOUSBOE P, GHILADI M, RASMUSSEN L, 1992. Nutritional stress relieved by addition of hemin and phospholipids. J Comp Physiol B 162: 107-110.
9. CHRISTENSEN ST, SCHOUSBOE P, NIELSEN D, SØNDERGAARD G, RASMUSSEN L, 1993. Cell multiplication in Tetrahymena setosa and Tetrahymena thermophila in synthetic nutrient medium. Effects of ethanol, cholesterol and extracellular medium. Acta Protozool 32: 151-156.
10. CHRISTENSEN ST, WHEATLEY DN, RASMUSSEN MI, RASMUSSEN L, 1995b. Mechanisms controlling death, survival and proliferation in a model unicellular eukaryote cell system, Tetrahymena thermophila. Cell Death Diff 2: 301-308.
11. CHRISTOPHER GK, SUNDERMAN CA, 1992. Conventional and confocal microscopic studies of insulin receptor induction in Tetrahymena pyriformis. Exp Cell Res 201: 477-484.
12. CSABA G, 1994. Phylogeny and ontogeny of chemical signalling: origin and development. Int Rev Cytol 155: 1-48.
13. ELION EA, 1995. Ste5: a meeting place for MAP kinases and their associates. Trends in Cell Biol 5: 322-327.
14. FEELISCH M, NOACK EA, 1987. Correlation between nitric oxide formation during degradation of organic nitrates and activation of guanylate cyclase. Eur J Pharmacol 139: 19-30.
15. FORSTERMANN U, SCHMIDT HHHW, POLLOCK JS, HELLER M, MURAD F, 1991. Enzymes synthesizing guanylate cyclase-activating factors in endothelial cells, neuroblastoma cells and rat brain. J Cardiovasc Pharmacol 17: S57-S64.
16. GARBERS DL, 1992. Guanylyl cyclase receptors and their endocrine, paracrine and autocrine ligands. Cell 17: 1-4.
17. GERISCH G, 1986. Interelation of cell adhesion and differentiation in Dictyostelium discoideum. J Cell Sci Suppl 4: 201-219.
18. GERISCH G, 1987. Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium. Ann Rev Biochem 56: 853-879.
19. GERZER R, BRASH AR, HARDMAN JG, 1986. Activation of soluble guanylate cyclase by arachidonic acid and 15-lipooxygenase products. Biochim Biophys Acta 886: 383-389.
20. GERZER R, HAMET P, Ross AH, LAWSON JA, HARDMAN JG, 1983. Calcium-induced release from platelet membranes of fatty acids that modulate soluble guanylate cyclase. J Pharmacol Exp Ther 226: 180-186.
21. GLASS DB, FREY II W, CARR DW, GOLDBERG ND, 1977. Stimulation of human platelate guanylate cyclase by fatty acids. J Biol Chem 252: 1279-1285.
22. G-methyl-L-arginine causes endothelium-dependent contraction and inhibition of cyclic GMP formation in artery and vein. Proc Natl Acad Sci USA 87: 4430-4434.
23. GRAVE M, HAGEMEISTER JJ, KRISTIANSEN TB, LYHNE I, HELLUNG-LARSEN P, 1995. Growth factor removal from Tetrahymena cells leads to cell death at the medium/air interphase. Proc 4th Asian Conf Ciliate Biol 22-45.
24. GRAVES MG, DICKINSON JR, SWOBODA BEP, 1976. Cyclic GMP and cyclic GMP phosphodiesterase in the cell cycle of Tetrahymena pyriformis. FEBS Lett 69: 165-166.
25. +-ATPase activity by nitric oxide: a cGMP-independent effect. Am J Physiol 266: H2146-H2151.
26. HOLZ GG JR, ERWIN S, ROSENBAUM N, AARONSON S, 1973. Triparanol inhibition of Tetrahymena and its prevention by lipids. Arch Biochem Biophys 98: 312-322.
27. IGNARRO LJ, 1992. Haem-dependent activation of cytosolic guanylate cyclase by nitric oxide: a widespread signal transduction mechanism. Biochem Soc Trans 20: 465-469.
28. IGNARRO LJ, LIPPTON HL, EDWARDS JC, BARRICOS WH, HYMAN AL, 1981. Mechanisms of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: evidence for the involvement of S-nitrosothiols as active intermediates. J Pharmacol Exp Ther 218: 739-749.
29. IGNARRO LJ, WOOD KS, WOLIN MS, 1984. Regulation of purified soluble guanylate cyclase by porphyrins and metalloporphyrins: a unifying concept. Adv Cyclic Nucleotide Protein Phosphorylation Res 17: 267-274.
30. ISHII DN, MANIATIS GM, 1978. Haemin promotes rapid neurite outgrowth in cultured mouse neuroblastoma cells. Nature 274: 372-374.
31. JANSSENS PMW, 1987. Did vertebrate signal transduction mechanisms originate in eukaryote microbes? TIBS 12: 456-459.
32. KIDDER GW, DEWEY VC, 1951. The biochemistry of ciliates in pure culture. In Lwoff A, ed. Biochemistry and Physiology of Ciliates 1. Academic Press. New York and London, pp. 323-400.
33. KÖHIDAI L, BARSONY J, ROTH J, MARX SJ, 1992. Rapid effects of insulin on cyclic GMP location in an intact protozoan. Experientia 40: 476-481.
34. KOVACS P, CSABA G, 1990. Evidence of the receptor nature of the binding sites induced in Tetrahymena by insulin treatment. A quantitive cytofluoremetric technique for the study of binding kinetics. Cell Biochem Fund 8: 49-56.
35. KOVACS P, CSABA G, NAGAO S, NOZAWA Y, 1989. The regulatory role of calmodulin-dependent guanylate cyclase in association with hormonal imprinting in Tetrahymena Microbios 59: 123-128.
36. LEROITH D, LIOTTA AS, ROTH J, SHILOACH J, LEWIS ME, PERT CB, KRIEGER DT, 1982. Corticotrophin and b-endorphin-like materials are native to unicellular organisms. Proc Natl Acad Sci USA 79: 2086-2090.
37. LEROITH D, SHILOACH J, ROTH J, LESNIAK MA, 1980. Evolutionary origins of vertebrate hormones: substances similar to mammalian insulins are native to unicellular organisms. Proc Natl Acad Sci USA 77: 6184-6188.
38. LIU G, NEWELL PC, 1988. Evidence that cGMP regulates myosin interaction with the cytoskeleton during chemotaxis of Dictyostelium. J Cell Sci 90: 123-129.
39. LUO D, DAS S, VINCENT SR, 1995. Effects of methylene blue and LY83583 on neuronal nitric oxide synthase and NADPH-diaphorase. Eur J Pharmacol 290: 247-251.
40. MALTA E, 1989. Biphasic relaxant curves to glycerol trinitrate in rat aortic rings. Naunyn-Schmiedeberg's Arch Pharmacol 339: 236-243.
41. MARTIN W, VILLANI GM, JOTHIANANDAN D, FURCHGOTT RF, 1985. Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther 232: 708-716.
42. MAYER B, BRUNNER F, SCHMIDT K, 1993. Inhibition of nitric oxide synthesis by methylene blue. Biochem Pharmacol 45: 367-374.
43. MAYEUX P, FELIX J-M, BILLAT C, JACQUOT R, 1986. Induction by hemin of proliferation and differentiation of progenitor erythroid cells responsible for erythropoitin. Exp Hematol 14: 801-808.
44. MONCADA S, PALMER RMJ, HIGGS EA, 1991. Nitric oxide: physiology, patophysiology and pharmacology. Pharmacol Rev 43: 109-142.
45. MULSCH A, BUSSE R, LIEBAU S, FORSTERMANN U, 1988. LY83583 interferes with the release of endothelium-derived relaxing factor and inhibits soluble guanylate cyclase. J Pharmacol Exp Ther 247: 283-288.
46. MUROFUSHI H, 1973. Purification and characterization of a protein kinase in Tetrahymena. Biochem Biophys Acta 327: 354-364.
47. MUROFUSHI H, 1974. Protein kinases in Tetrahymena cilia. II. Partial purification and characterization of adenosine 3′,5′-monophosphate-dependent and guanosine 3′,5′-monophosphate-dependent protein kinases. Biochem Biophys Acta 370: 130-139.
48. NATHAN C, 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J 6: 3051-3064.
49. NOVOGRODSKY A, SUTHANTHIRAN M, STENZEL KH, 1991. Ferro-mitogenes: iron-containing compounds with lymphocyte-stimulatory properties. Cell Immunol 133: 295-305.
50. O'NEIL JB, PERT CB, RUFF MR, SMITH CC, HIGGINS WJ, ZIPSER B, 1988. Identification and characterization of the opiate receptor in the ciliated protozoan, Tetrahymena. Brain Res 450: 303-315.
51. ORIAS E, BRUNS PJ, 1976. Induction and isolation of mutants in Tetrahymena. In: Prescott DM, ed. Methods in Cell Biology. Academic Press. New York, pp. 247-282.
52. PARFENOVA EV, AFON'KIN SY, YUDIN AL, ETINGOF RN, 1989. Characterization and partial purification of mating pheromone excreted by mating type II cells of the ciliate Dileptus anser. Acta Protozool 28: 11-21.
53. PAVETO C, PEREIRA C, ESPINOSA J, et al., 1995. The nitric oxide transduction pathway in Trypanosoma cruzi. J Biol Chem 270: 16,576-16,579.
54. RANDRIAMAMPITA C, CIAPA B, TRAUTMANN A, 1991. Cyclic GMP-dependent refilling of calcium stores in macrophages. Eur J Physiol 417: 633-637.
55. RÖSEN R, KÖNIG E, KLAUS W, 1987. Different sensitivities of arteries and veins to glyceryltrinitrate-induced relaxation and tolerance: an 'in vitro' study on isolated vessels from rabbits. Arch Int Pharmacodyn Ther 285: 226-237.
56. SCHMIDT MJ, SAWYER BD, TRUEX LL, MARSHALL WS, FLEISH JH, 1985. LY83583: an agent that lowers intracellular levels of cyclic guanosine 3′,5-monophosphate. J Pharmacol Exp Ther 232: 764-769.
57. SCHOUSBOE P, CHRISTENSEN ST, GHILADI M, RASMUSSEN L, 1992. Porphyrin rings and phospholipids: stimulators of cloning efficiency in certain species of Tetrahymena. J Protozool 39: 343-345.
58. SCHOUSBOE P, RASMUSSEN L, 1994. Survival of Tetrahymena thermophila at low initial cell densities; effects of lipids and long-chain alcohols. J Euk Microbiol 41: 195-199.
59. SCHULTZ JE, KLUMPP S, 1980. Guanylate cyclase in the excitable ciliary membrane of Paramecium. FEBS Lett 122: 64-66.
60. SCHULTZ JE, KLUMPP S, 1984. Calcium/calmodulin-regulated guanylate cyclase in the ciliary membranes of Paramecium and Tetrahymena. Adv Cyclic Nucleotide Protein Phosphorylation Res 17: 275-283.
61. SCHULTZ JE, KLUMPP S, 1994. Cyclic GMP in lower forms. Adv Pharmacol 26: 285-303.
62. SHILOACH J, RUBINOVITZ C, LEROITH D, 1985. Extractions of insulin-related material and other peptide-hormones from Tetrahymena pyriformis. ACS Symp Ser 271: 175-191.
63. STAMLER JS, SINGEL DJ, LOSCALZO J, 1992. Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902.
64. SZABLEWSKI L, ANDRESEN PH, FLORIN-CHRISTENSEN J, FLORIN-CHRISTENSEN M, RASMUSSEN L, 1991. Tetrahymena thermophila: growth in synthetic medium in the presence and absence of glucose. J Protozool 38: 62-65.
65. TAGAKI Y, NIMURA K, KINOSHITA H, YAMADA T, KAJI K, TANABE H, 1989. Identification of a gene that shortens clonal life span of Paramecium tetraurelia. Genetics 123: 749-754.
66. TAGAKI Y, NIMURA K, TOKUSUMI Y, FUJISAWA H, KAJI K, TANABE H, 1993. Secretion of mitogenic factor(s) from stocks of Paramecium tetraurelia, P. caudatum and P. multimicronucleatum. Zool Sci 10: 53-56.
67. TANABE H, NISHI N, TAGAKI Y, NADA F, AHATMATSU I, KAJI K, 1990. Purification and identification of a growth factor by Paramecium tetraurelia. Biochem Biophys Res Commun 170: 786-792.
68. TAO Y, HOWLETT A, KLEIN C, 1992a. Nitric oxide-releasing compounds inhibit Dictyostelium discoideum aggregation without altering cGMP production. FEBS 314: 49-52.
69. TAO Y, HOWLETT A, KLEIN C, 1992b. Nitric oxide stimulates the ADP-ribosylation of a 41-kDa cytosolic protein in Dictyostelium discoideum. Proc Natl Acad Sci USA 89: 5902-5906.
70. TSAI SC, ADAMIK R, MANGANIELLO VC, VAUGHAN M, 1983. Regulation of activity of purified guanylate cyclase from liver that is unresponsive to nitric oxide. Biochem J 215: 447-455.
71. VALLESI A, GIOVANNA G, BRADSHAW RA, LUPORINI P, 1995. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 376: 522-524.
72. WALDMAN SA, MURAD F, 1987. Cyclic GMP synthesis and function. Pharmacol Rev 39: 163-196.
73. WALDMAN SA, SINACORE MS, LEWICKI JA, CHANG LY, MURAD F, 1984. Selective activation of particulate guanylate cyclase by a specific class of porphyrins. J Biol Chem 259: 4038-4042.
74. WHEATLEY DN, CHRISTENSEN ST, SCHOUSBOE P, RASMUSSEN L, 1993. Signalling in cell growth and death: adequate nutrition alone may not be sufficient for ciliates. Cell Biol Int 17: 817-823.
75. WHITBREAD JA, SIMS M, KATZ ER, 1991. Evidence for the presence of a growth factor in Dictyostelium discoideum. Dev Gen 12: 78-81.
76. WOLIN M, CHERRY PD, RODENBERG JM, MESSINA EJ, KALEY G, 1990. Methylene blue inhibits vasodilation of skeletal muscle arterioles to acetylcholine and nitric oxide via the extracellular generation of Superoxide anion. J Pharmacol Exp Ther 254: 872-876.
77. ZWILLER J, BASSET P, ULRICH G, MANDEL P, 1982. Guanylate cyclase activators hemin and sodium nitroprusside stimulate cell growth in serum-free medium. Exp Cell Res 141: 445-449.