RAP1A GTP/GDP cycles determine the intracellular location of the late endocytic compartments and contribute to myogenic differentiation

Experimental Cell Research

Volumn 246, Issue 1, 1999, Pages 56-68

  Pizon, Véronique ^a   Méchali, Francisca ^b   Baldacci, Giuseppe ^a  

^a CNRS   (France)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

Late endosome; Lysosomes; Myogenic differentiation; RAP1A; Ras like protein

Indexed keywords

CATHEPSIN D; CELL PROTEIN; GUANOSINE TRIPHOSPHATE; MYOGENIN; RAP1A PROTEIN; RAS PROTEIN; TROPONIN T; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL ULTRASTRUCTURE; ENDOCYTOSIS; MUSCLE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALIA;

EID: 0344631664     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1998.4284     Document Type: Article

References (61)

1. Okazaki K., Holtzer H. Myogenesis:fusion, myosin synthesis and the mitotic cycle. Proc. Natl. Acad. Sci. USA. 56:1966;1484-1488.
2. Nadal-Ginard B. Commitment, fusion and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis. Cell. 15:1978;855-864.
3. Olson E. Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154:1992;261-272.
4. Lassar A., Skapek S., Novitch B. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6:1994;788-794.
5. Devlin R., Emerson C. Coordinate accumulation of contractile protein synthesis during myoblast differentiation. Cell. 13:1978;599-611.
6. Bird J., Roisen F. Lysosomes in muscles: developmental aspects, enzyme activities and role in protein turnover. Myology: Basic and Clinical. Part 1. The Anatomy, Physiology and Biochemistry of Muscle. 1986;McGraw-Hill, New York. p. 745-767.
7. Ralston E. Changes in architecture of the Golgi complex and other subcellular organelles during myogenesis. J. Cell Biol. 120:1993;399-409.
8. Kirschke H., Wood L., Roisen F., Bird J. Activity of lysosomal cysteine protease during differentiation of rat skeletal muscle. Biochem. J. 214:1983;871-877.
9. Béchet D., Ferrara M., Mordier S., Roux M. P., Deval C., Obled A. Expression of lysosomal cathepsin B during calf myoblast-myotube differentiation. J. Biol. Chem. 266:1991;14104-14112.
10. Jane D., Dufresne M. Expression and regulation of three lysosomal cysteine protease activities during growth of the differentiating L6 rat myoblast cell line and its nonfusing variant. Biochem. Cell Biol. 72:1994;267-274.
11. Gogos J., Thompson R., Lowry W., Sloane B., Weintraub H., Horwitz M. Gene trapping in differentiating cell lines: Regulation of the lysosomal protease Cathepsin B in skeletal myoblast growth and fusion. J. Cell Biol. 134:1996;837-847.
12. Griffiths G., Hoflack B., Simons K., Mellman I., Kornfeld S. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52:1988;329-341.
13. Butor C., Griffiths G., Aronson N., Varki A. Co-localization of hydrolytic enzymes with widely disparate pH optima: Implications for the regulation of lysosomal pH. J. Cell Sci. 108:1995;2213-2219.
14. Pizon V., Chardin P., Lerosey I., Olofsson B., Tavitian A. Human cDNAs rap1 and rap2 homologous to the drosophila gene Dras3 encode proteins closely related to ras in the 'effector' region. Oncogene. 3:1988;201-204.
15. Van den Berghe N., Cool R., Horn G., Wittinghofer A. Biochemical characterization of C3G: An exchange factor that discriminates between Rap1 and Rap2 and is not inhibited by Rap1A(S17N). Oncogene. 15:1997;845-850.
16. Rubinfeld B., Munemitsu S., Clark R., Conroy L., Watt K., Crosier W., McCormick F., Polakis P. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21 rap1. Cell. 65:1991;1033-1042.
17. Weinecke R., König A., DeClue J. Identification of Tuberin, the tuberous sclerosis-2 product. J. Biol. Chem. 27:1995;16409-16414.
18. Cullen P. J., Hsuan J. J., Truong O., Letcher A. J., Jackson T. R., Dawson A. P., Irvine R. F. Identification of a specific Ins(1,3,4,5)P4-binding protein as a member of the GAP1 family. Nature. 376:1995;527-530.
19. Kaibuchi K., Mizuno T., Fujioka H., Yamamoto T., Kishi K., Fukumoto Y., Hori Y., Takai Y. Molecular cloning of the cDNA for stimulatory GDP/GTP exchange protein for smg p21s (ras p21-like small GTP-binding proteins) and characterization of stimulatory GDP/GTP exchange protein. Mol. Cell Biol. 11:1991;2873-2880.
20. Gotoh T., Hattori S., Nakamura S., Kitayama H., Noda M., Takai Y., Kaibuchi K., Matsui H., Hatase O., Takahashi H., Kurata T., Matsuda M. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol. Cell Biol. 15:1995;6746-6753.
21. Nassar M., Horn G., Herrmann C., Scherer A., McCormick F., Wittinghofer A. The 2.2 angstrom crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature. 375:1995;554-560.
22. Frech M., John J., Pizon V., Chardin P., Tavitian A., Clark R., McCormick F., Wittinghofer A. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science. 249:1990;169-171.
23. Spaargaren M., Bischoff J. R. Identification of the guanine nucleotide dissociation stimulator for Ral as a putative effector molecule of R-ras, H-ras, K-ras, and Rap. Proc. Natl. Acad. Sci. USA. 91:1994;12609-12613.
24. Ikeda M., Koyama S., Okazaki M., Dohi K., Kikuchi A. rap1 p21 regulates the interaction of ras p21 with RGL, a new effector protein of ras p21. FEBS Lett. 375:1995;37-40.
25. Wolthuis R., Bauer B., Vantveer L., Devriessmits A., Cool R., Spaargaren M., Wittinghofer A., Burgering B., Bos J. RalGDS-like factor (Rlf) is a novel Ras and Rap 1A-associating protein. Oncogene. 13:1996;353-362.
26. Serebriiskii I., Estojak J., Sonoda G., Testa J., Golemis E. Association of Krev/rap1a with Krit1, a novel ankyrin repeat-containing protein encoded by a gene mapping to 7q21-22. Oncogene. 15:1997;1043-1049.
27. Vavvas D., Li X., Avruch J., Zhang X. Identification of Nore1 as a potential Ras effector. J. Biol. Chem. 273:1998;5439-5442.
28. Kitayama H., Sugimoto Y., Matsuzaki T., Ikawa Y., Noda M. A ras-related gene with transformation suppressor activity. Cell. 56:1989;77-84.
29. Pizon V., Desjardins M., Bucci C., Parton R. G., Zerial M. Association of Rap1a and Rap1b proteins with late endocytic/phagocytic compartments and Rap2a with the Golgi complex. J. Cell Sci. 107:1994;1661-1670.
30. Pizon V., Cifuentes-Diaz C., Mege R. M., Baldacci G., Rieger F. Expression and localization of RAP1 proteins during myogenic differentiation. Eur. J. Cell Biol. 69:1996;224-235.
31. Gossen M., Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA. 89:1992;5547-5551.
32. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:1977;725-727.
33. Herrmann C., Horn G., Spaargaren M., Wittinghofer A. Differential interaction of the Ras family GTP-binding proteins H-Ras, Rap1a, and R-Ras with the putative effector molecules Raf kinase and Ral-guanine nucleotide exchange factor. (1996). J. Biol. Chem. 271:1996;6794-6800.
34. Anderson R., Orci L. A view of acidic intracellular compartments. J. Cell Biol. 106:1988;539-543.
35. Vitelli R., Santillo M., Lattero D., Chiariello M., Bifulco M., Bruni C., Bucci C. Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272:1997;4391-4397.
36. Bucci C., Parton R., Mather I., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 function as a regulatory factor in the endocytic pathway. Cell. 70:1992;715-728.
37. Stenmark H., Parton R., Steele-Mortimer O., Lücke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase stimulates membrane fusion and endocytosis. EMBO J. 13:1994;1287-1296.
38. Franke B., Akkerman J., Bos J. Rapid Ca2+ -mediated activation of Rap1 in human platelets. EMBO J. 16:1997;252-259.
39. Breitbart R., Nguyen H., Medford R., Destree A., Mahdavi V., Nadal-Ginard B. Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell. 41:1995;67-82.
40. Wright W., Sassoon D., Lin V. Myogenin, a factor regulating myogenesis has a domain homologous to MyoD. Cell. 56:1989;607-617.
41. Crescenzi M., Crouch D., Tato F. Transformation by myc prevents fusion but not biochemical differentiation of C2C12 myoblasts: Mechanisms of phenotypic correction in mixed culture with normal cells. J. Cell Biol. 125:1994;1137-1145.
42. Chavrier P., Parton R., Hauri H., Simons K., Zerial M. Localisation of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:1990;317-329.
43. Hasilik A. The early and late processing of lysosomal enzymes: Proteolysis and compartimentation. Experientia. 48:1992;130-151.
44. Zerial M., Stenmark H. Rab GTPases in vesicular transport. Curr. Opin. Cell Biol. 5:1993;613-620.
45. Méresse S., Gorvel J. P., Chavrier P. The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J. Cell Sci. 108:1995;3349-3358.
46. York R., Yao H., Dillo T., Ellig C., Eckert S., McCleskey E., Stork P. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature. 392:1998;622-626.
47. Campbell J., Wenderoth M., Hauschka S., Krebs E. Differential activation of mitogen-activated protein kinase in response to basic fibroblast growth factor in skeletal muscle cells. Proc. Natl. Acad. Sci. USA. 92:1995;870-874.
48. Kudla A., John M., Bowen-Pope D., Rainish B., Olwin B. A requirement for fibroblast growth factor in regulation of skeletal muscle growth and differentiation cannot be replaced by activation of platelet-derived growth factor signaling pathways. Mol. Cell. Biol. 15:1995;3238-3246.
49. Milasincic D., Calera M., Farmer S., Pilch P. Stimulation of C2C12 myoblast growth by basic fibroblast growth factor and insulin-like growth factor 1 can occur via mitogen activated protein kinase-dependent and independent pathways. Mol. Cell. Biol. 16:1996;5964-5973.
50. Mourey R., Vega Q, Campbell J., Wenderoth M., Hauschka S., Krebs E., Dixon J. A novel cytoplasmic dual specific protein tyrosine phosphatase implicated in muscle and neuronal differentiation. J. Biol. Chem. 271:1996;3795-3802.
51. Weyman C., Ramocki M., Taparowsky E., Wolfman A. Distinct signaling pathways regulate transformation and inhibition of skeletal muscle differentiation by oncogenic Ras. Oncogene. 14:1997;697-704.
52. Bennett A., Tonks N. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science. 278:1997;1288-1291.
53. Feig L., Cooper G. Inhibtion of NIH3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8:1988;3235-3243.
54. Maly F., Quilliam L., Dorseuil O., Der C., Bokoch G. Activated or dominant inhibitory mutants of Rap1A decrease the oxidative burst of Epstein-Barr virus transformed human B lymphocytes. J. Biol. Chem. 269:1994;18743-18746.
55. Gabig T., Crean C., Mantel P., Rosi R. Function of wild-type or mutant Rac2 and Rap1a GTPases in differentiated HL60 cell NADPH oxidase activation. Blood. 85:1995;804-811.
56. Vossler M., Yao H., York R., Pan M., Rim C., Stork P. cAMP activates MAP kinase and Elk-1 through a B-Raf and Rap1-dependent pathway. Cell. 89:1997;73-82.
57. Kitayama H., Matsuzaki T., Ikawa Y., Noda M. Genetic analysis of the Kirsten-ras-revertant 1 gene: Potentiation of its tumor suppressor activity by specific point mutations. Proc. Natl. Acad. Sci. USA. 87:1990;4284-4288.
58. Park H-O., Bi E., Pringle J., Herskowitz I. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc. Natl. Acad. Sci. USA. 94:1997;4463-4468.
59. Schwartz W. N., Bird J. W. C. Degradation of myofibrillar proteins by cathepsins B and D. Biochem. J. 167:1977;811-820.
60. Tjelle E., Brech A., Juvet K., Griffiths G., Berg T. Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: Their role in protein degradation. J. Cell Sci. 109:1996;2905-2914.
61. Edmonson D., Olson E. Helix-loop-helix proteins as regulators of muscle-specific transcription. J. Biol. Chem. 268:1993;755-758.