Granule lattice protein 1 (Grl1p), an acidic, calcium-binding protein in tetrahymena thermophila dense-core secretory granules, influences granule size, shape, content organization, and release but not protein sorting or condensation

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1775-1787

  Chilcoat, N Doane ^a   Melia, Sharon M ^a   Haddad, Alex ^a   Turkewitz, Aaron P ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b THE UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM BINDING PROTEIN;

ARTICLE; CELL AGGREGATION; CELL MEMBRANE PERMEABILITY; CILIATE; GENE MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TETRAHYMENA THERMOPHILA;

ACIDS; ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; BLOTTING, NORTHERN; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CLONING, MOLECULAR; CYTOPLASM; CYTOPLASMIC GRANULES; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TETRAHYMENA THERMOPHILA; TRANSCRIPTION, GENETIC;

EID: 0030478918     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1775     Document Type: Article

References (94)

1. Adoutte, A. 1988. Exocytosis: biogenesis, transport and secretion of trichocysts. In Paramecium. H.D. Gortz, editor. Springer-Verlag, Berlin. 325-362.
2. Adoutte, A., N. Carreau de Loubresse, and J. Beisson. 1984. Proteolytic cleavage and maturation of the crystalline secretion products at Paramecium. J. Mol. Biol. 180:1065-1081.
3. Almers, W. 1990. Exocytosis. Annu. Rev. Physiol. 52:607-624.
4. Anderson, R.G.W., and L. Orci. 1988. A view of acidic intracellular compartments. J. Cell Biol. 106:539-543.
5. Attanoos, R.L., and A.K. Allen. 1987. The characterization of the proteins which are secreted by the mucocysts of Tetrahymena thermophila. Biochim. Biophys. Acta. 924:154-158.
6. Aufderheide, K.J. 1978. The effective sites of some mutations affecting exocytosis in Paramecium tetraurelia. Mol. Gen. Genet. 165:199-205.
7. Azaryan, A.V., T.J. Krieger, and V.Y. Hook. 1995. Purification and characteristics of the candidate prohormone processing proteases PC2 and PC1/3 from bovine adrenal medulla chromaffin granules. J. Biol. Chem. 270: 8201-8208.
8. Bailyes, E.M., K.I. Shennan, A.J. Seal, S.P. Smeekens, D.F. Steiner, J.C. Hutton, and K. Docherty. 1992. A member of the eukaryotic subtilisin family (PC3) has the enzymic properties of the type 1 proinsulin-converting endopeptidase. Biochem. J. 285:391-394.
9. Beisson, J., M. Lefort-Tran, M. Pouphile, M. Rossignol, and B. Satir. 1976. Genetic analysis of membrane differentiation in Paramecium: freeze-fracture study of the trichocyst cycle in wild-type and mutant strains. J. Cell Biol. 69:126-143.
10. 2+-mediated event during the final steps of exocytosis in Paramecium cells. J. Cell Biol 88:179-188.
11. Bonnemain, H., T. Gulik-Krzywicki, C. Grandchamp. and J. Cohen. 1992. Interactions between genes involved in exocytotic membrane fusion in Paramecium. Genetics. 130:461-470.
12. Bresslau, E. 1921. Die experimentalle Erzeugung von Hullen bei Infusorien als Parallele zur Membranbildung bei der kunstlichen Parthenogenese. Naturwissenschaften. 9:57-62.
13. Bruns, P.J. 1986. Genetic organization of Tetrahymena. In The Molecular Biology of Ciliated Protozoa. J. Gall, editor. Academic Press, New York. 27-44.
14. Bruns, P.J., and T.B. Brussard. 1974. Positive selection for mating with functional heterokaryons in Tetrahymena pyriformis. Genetics. 78:831-841.
15. Burgess, T.L., and R.B. Kelly. 1987. Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:243-293.
16. Burgoyne, R.D. 1991. Control of exocytosis in adrenal chromaffin cells. Biochim. Biophys. Acta. 1071:174-202.
17. Camell, L., and H.-P.H. Moore. 1994. Transport via the regulated secretory pathway in semi-intact PC12 cells: role of intra-cisternal calcium and pH in the transport and sorting of secretogranin II. J. Cell Biol. 127:693-705.
18. Cathala, G., J.F. Savouret, B. Mendez, B.L. West, M. Karin, J.A. Martial, and J.D. Baxter. 1983. A method for the isolation of intact, translationally active ribonucleic acid. DNA. 2:329-335.
19. Chanat, E., and W.B. Huttner. 1991. Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J. Cell Biol. 115:1505-1519.
20. Chandra, S., E.P.W. Kable, G.H. Morrison, and W.W. Webb. 1991. Calcium sequestration in the Golgi apparatus of cultured mammalian cells revealed by laser scanning confocal microscopy and ion microscopy. J. Cell Sci. 100:747-752.
21. Cole, E.S., and P.J. Bruns. 1993. Uniparental cytogamy: a novel, efficient method for bringing mutations of Tetrahymena into homozygous expression with precocious sexual maturity. Genetics. 132:1017-1031.
22. Cole, E.S., and K.R. Stuart. 1991. Biochemical and cytological evidence for an overabundance of mucocysts in the bed pattern mutant of Tetrahymena thermophila. J. Protozool. 38:536-547.
23. Collins, T., and J.M. Wilhelm. 1981. Post-translational cleavage of mucocyst precursors in Tetrahymena, J. Biol. Chem. 256:10475-10484.
24. Colomer, V., G.A. Kicska, and M.J. Rindler. 1996. Secretory granule content proteins and the luminal domains of granule membrane proteins aggregate in vitro at mildly acidic pH J. Biol. Chem. 271:48-55.
25. Conway, J.F., and D.A.D. Parry. 1990. Structural features in the heptad substructure and longer range repeats of two-stranded α-fibrous proteins. Int. J. Biol. Macromol. 12:328-334.
26. Davidson, H.W., C.J. Rhodes, and J.C. Hutton. 1988. Intraorganellar calcium and pH control proinsulin cleavage in the pancreatic β cell via two distinct site-specific endopeptidases. Nature (Lond.). 333:93-96.
27. Ding, Y., A. Ron, and B.H. Satir. 1991. A potential mucus precursor in Tetrahymena wild type and mutant cells. J. Protozool. 38:613-623.
28. Docherty, K., and D.F. Steiner. 1982. Post-translational proteolysis in polypeptide hormone biosynthesis. Annu. Rev. Physiol. 44:625-638.
29. Farquhar, M.G., and G.E. Palade. 1981. The Golgi apparatus (complex)-(1954-1981)-from artifact to center stage. J. Cell Biol. 91:77s-103s.
30. Farrell, R.E.J. (1993). RNA Methodologies: A Laboratory Guide for the Isolation and Characterization. Academic Press. New York. 126-204.
31. Fisher, J.M., W. Sossin, R. Newcomb, and R.H. Scheller. 1988. Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell. 54:813-822.
32. Gaertig, J., and M. A. Gorovsky. 1992. Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc. Natl. Aanl. Sci. USA. 89:9196-9200.
33. Gaerlig, J., T.H. Thatcher, K.E. McGrath, R.C. Callahan, and M.A. Gorovsky. 1993. Perspectives on tubulin isotype function and evolution based on the observation that Tetrahymena thermophila microtubules contain a single alpha- and beta-tubulin. Cell Motil. Cytoskel. 25:243-253.
34. Gaertig, J., L. Gu, B. Hai, and M.A. Gorovsky. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucl. Acids Res. 22:5391-5398.
35. Gaertig, J., T.H. Thatcher, and M.A. Gorovsky. 1995. Gene transfer by electroporation of Tetrahymena. In Electroporation Protocols for Microorganisms. J.A. Nickoloff. editor. Humana Press, Totawa, NJ. 331-348.
36. Garreau de Loubresse, N. 1993. Early steps of the secretory pathway in Paramecium. In Membrane Traffic in Protozoa. JAI Press, Greenwich, CT. 27-60.
37. Garreau de Loubresse, N., M.-C. Gautier, and L. Sperling. 1994. Immature secretory granules are not acidic in Paramecium: implications for sorting to the regulated pathway. Biol. Cell. 82:139-147.
38. Gautier, M.-C., L. Sperling, and L. Madeddu. 1996. Cloning and sequence analysis of genes coding for Paramecium secretory granule (trichocyst) proteins. J. Biol. Chem. 271:10247-10255.
39. Gerdes, H.-H., P. Rosa, E. Phillips, P.A. Baeuerle, R. Frank, P. Argos, and W.B. Huttner. 1989. The primary structure of human secretogranin II. a widespread tyrosine-sulfated secretory granule protein that exhibits low pH - and calcium-induced aggregation. J. Biol Chem. 264:12009-12015.
40. Gorr, S.-U., W.L. Dean, T.L. Radley, and D.V. Cohn. 1988. Calcium-binding and aggregation properties of parathyroid secretory protein-I (chromogranin A). Bone Miner. 4:17-25.
41. Gorr, S.-U., J. Shioi, and D.V. Cohn. 1989. Interaction of calcium with porcine adrenal chromogranin (secretory protein-I) and chromogranin B (secretogranin I). Am. J. Physiol. 257:E247-E254.
42. Gutierrez, J.C., and E. Orias. 1992. Genetic characterization of Tetrahymena thermophila mutants unable to secrete capsules. Dev. Genet. 13: 160-166.
43. Hausmann, K. 1972. Cytologische Studien an Trichocysten. IV. - die Feinstruktur ruhender und ausgeschiedener Protrichocysten von Loxophyllum, Tetrahymena, Prorodon und Lacrymaria. Protistologica. 8:401-412.
44. Hausmann, K. 1978. Extrusive organelles in protists. Int. Rev. Cytol. 52: 197-276.
45. Hausmann, K., A.K. Fok, and R.D. Allen. 1988. Immunocytochemical analysis of trichocyst structure and development in Paramecium. J. Ultrastruct. Mol. Struct. Res. 99:213-225.
46. Horowitz, S., J.K. Bowen, G.A. Bannon, and M.A. Gorovsky. 1987. Unusual features of transcribed and translated regions of the histone H4 gene family of Tetrahymena thermophila. Nucleic Acids Res. 15:141-160.
47. Huttner, W.B., and S.A. Tooze. 1989. Biosynthetic protein transport in the secretory pathway. Curr. Opin. Cell Biol. 1:648-654.
48. Kahn, R.W., B.H. Andersen, and C.F. Brunk. 1993. Transformation of Tetrahymena thermophila by microinjection of a foreign gene. Proc. Natl. Acad. Sci. USA. 90:9295-9299.
49. Kelly, R.B. 1985. Pathways of protein secretion in eukaryotes. Science (Wash. DC). 230:25-32.
50. Kerboeuf, D., A. Le Berre, J.-C. Dedieu, and J. Cohen. 1993. Calmodulin is essential for assembling links necessary for exocytic membrane fusion in Paramecium. EMBO (Eur. Mol. Biol. Organ.) J. 12:3385-3390.
51. Kuliawat, R., and P. Arvan. 1992. Protein targeting via the "constitutive-like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule compartment. J. Cell Biol. 118:521-529.
52. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly of the head of hacteriophage T4. Nature (Lond.). 227:680-682.
53. Lefort-Tran, M., K. Aufderheide, M. Pouphile, M. Rossignol, and J. Beisson. 1981. Control of exocytic processes: cytological, and physiological studies of trichocyst mutants in Paramecium tetraurelia. J. Cell Biol. 88: 301-311.
54. 52a. Lumpert, C.J., R. Glas-Albrecht, E. Eisenmann, and H. Plattner. 1992. Secretory organelles in Paramecium cells (trichocysts) are not remarkably acidic compartments. J. Histochem. Cytochem. 40:153-160.
55. Madeddu, L., M.-C. Gautier, L. Vayssié, A. Houari, and L. Sperling. 1995. A large multigenic family codes for the polypeptides of the crystalline trichocyst matrix in Paramecium. Mol. Biol. Cell. 6:649-659.
56. Maihle, N.J., and B.H. Satir. 1986. Protein secretion in Tetrahymena thermophila. Characterization of the major proteinaceous secretory proteins. J. Biol. Chem. 261:7566-7570.
57. Martindale, D.W. 1989. Codon usage in Tetrahymena, and other ciliates. J. Protozool. 36:29-34.
58. McDonald, B.B. 1966. The exchange of RNA and protein during conjugation in Tetrahymena. J. Protozool. 13:277-285.
59. Miller, S.G., and H.P. Moore. 1990. Regulated secretion. Curr. Opin. Cell Biol. 2:642-647.
60. Ochman, H., A.S. Gerber, and D.L. Hartl. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics. 120:621-623.
61. Orci, L., M. Ravazzola, and A. Perrelet. 1984. (Pro)insulin associates with Golgi membranes of pancreatic B cells. Proc. Natl Acad. Sci. USA. 81: 6743-6746.
62. Orci, L., M. Ravazzola, M. Amherdt, O. Madsen, J.-D. Vassalli, and A. Perrelet. 1985. Direct identification of prohormone conversion site in insulin-secreting cells. Cell. 42:671-681.
63. Orci, L., M. Ravazzola, M. Amherdt, A. Perrelet, S.K. Powell, D.L. Quinn, and H.-P.H. Moore. 1987. The trans-most cisternae of the Golgi complex: a compartment for sorting of secretory, and plasma membrane proteins. Cell. 51:1039-1051.
64. Orci, L., M. Ravazzola, M.-J. Storch, R.G.W. Anderson, J.-D. Vassalli, and A. Perrelet. 1987. Proteolytic maturation of insulin is a post-Golgi event which occurs in acidifying clathrin-coated secretory vesicles. Cell. 49: 865-868.
65. Orias, E., M. Flacks, and B.H. Satir. 1983. Isolation and ultrastructural characterization of secretory mutants of Tetrahymena thermophila. J. Cell Sci. 64:49-67.
66. Peck, R.K., B. Swiderski, and A.-M. Tourmel. 1993. Involvement of the trans-Golgi network, coated vesicles, vesicle fusion, and secretory product condensation in the biogenesis of Pseudomicrothorax trichocysts. In Membrane Traffic in Protozoa. H. Plattner, editor. JAI Press, Greenwich, CT. 1-26.
67. Plattner, H., C.J. Lumpen, G. Knoll, R. Kissmehl, B. Hohne, M. Momayezi, and A.R. Glas. 1991. Stimulus-secretion coupling in Paramecium cells. Eur. J. Cell Biol. 55:3-16.
68. Pollack, S. 1974. Mutations affecting the trichocysts in Paramecium aurelia. I. Morphology and description of the mutants. J. Protozool. 21:352-362.
69. Prescott, D.M. 1994. The DNA of ciliated protozoa. Microbiol. Rev: 58: 233-267.
70. Proudfoot, N.J., and E. Whitelaw. 1988. Termination and 3′ end processing of eukaryotic RNA. In Transcription and Splicing. B.D. Hames and B.M. Glover, editors. IRL Press. Oxford. 97.
71. Rindler, M.J. 1992. Biogenesis of storage granules and vesicles. Curr. Opin. Cell Biol. 4:616-622.
72. Rosendahl, G., P.H. Andreasen, and K. Kristiansen. 1991. Structure and evolution of the Tetrahymena thermophila gene encoding ribosomal protein L21. Gene. 98:161-167.
73. 70a. Ruiz, F., A. Adoutte, M. Rossignol, and J. Beisson. 1976. Genetic analysis of morphogenetic processes in Paramecium. Genet. Res. 27:109-122.
74. Russell, J.T. 1987. The secretory vesicle in processing and secretion of neuropeptides. Curr. Top. Membr. Transp. 31:277-312.
75. Sambrook, J., E.J. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. CSH Lab Press, Plainview, NY.
76. 72a. Sanford, J.C., F.D. Smith, and J.A. Russell. 1993. Optimizing the biolistic process for different biological applications. Methods Enzymol. 217:283-509.
77. Satir, B.H., M. Reichman, and E. Orias. 1986. Conjugation rescue of an exocytosis-competent membrane microdomain in Tetrahymena thermophila mutants. Proc. Natl. Acad. Sci. USA. 83:8221-8225.
78. Schmitz, M., R. Meyer, and K. Zierold. 1985. X-ray microanalysis in cryosections of natively frozen Paramecium caudatum with regard to ion distribution in ciliates. Scanning Electron Microsc. 1:443-445.
79. Schuel, H. 1978. Secretory functions of egg cortical granules in fertilization and development: a critical review. Gamete Res. 1:299-382.
80. Shennan, K.I.J., N.A. Taylor, and K. Docherty. 1994. Calcium- and pH-dependent aggregation and membrane association of the precursor of the prohormone convertase PC2. J. Biol. Chem. 269:18646-18650.
81. Sherman, F. 1991. Getting started with yeast. In Guide to Yeast Genetics and Molecular Biology. C. Guthrie and G.R. Fink, editors. Academic-Press, San Diego, CA. 3-20.
82. Steers, E., Jr., J. Beisson, and V.T. Marchesi. 1969. A structural protein extracted from the trichocysts of Paramecium aurelia. Exp. Cell Res. 57: 392-396.
83. Steiner, D.F. 1991. Prohormone convertases revealed at last. Curr. Biol. 1: 375-377.
84. Tiedtke, A. 1976. Capsule shedding in Tetrahymena. Naturwissenschaften. 63:93.
85. Tokuyasu, K., and O.H. Scherbaum. 1965. Ultrastructure of mucocysts and pellicle of Tetrahymena pyriformis. J. Cell Biol. 27:67-81.
86. Tooze, J., and S.A. Tooze. 1986. Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J. Cell Biol. 103:839-850.
87. Tooze, J., H.F. Kern, S.D. Fuller, and K.E. Howell. 1989. Condensationsorting events in the rough endoplasmic reticulum of exocrine pancreatic cells. J. Cell Biol. 109:35-50.
88. Tooze, S.A. 1991. Biogenesis of secretory granules. Implications arising from the immature secretory granule in the regulated pathway of secretion. FEBS J. 2:220-224.
89. Tooze, S.A., T. Flatmark, J. Tooze, and W.B. Huttner. 1991. Characterization of the immature secretory granule, an intermediate in granule biogenesis. J Cell Biol. 115:1491-1503.
90. Turkewitz, A.P., and R.B. Kelly. 1992. Immunocytochemical analysis of secretion mutants of Tetrahymena using a mucocyst-specific monoclonal antibody. Dev. Genet. 13:151-159.
91. Turkewitz, A.P., L. Madeddu, and R.B. Kelly. 1991. Maturation of dense core granules in wild type and mutant Tetrahymena thermophila. EMBO (Eur. Mol. Biol. Organ.) J. 10:1979-1987.
92. Von Heijne, G. 1983. Patterns of amino acids near signal-sequence cleavage sites. Eur. J. Biochem. 133:17-21.
93. Winkler, H., and R. Fischer-Colbrie. 1992. The chromogranins A and B: the first 25 years and future perspectives. Neuroscience. 3:497-528.
94. 2+-induced conformational change and aggregation of chromogranin A. J. Biol. Chem. 265:14414-14421.