Rac2, a hematopoiesis-specific Rho GTPase, specifically regulates mast cell protease gene expression in bone marrow-derived mast cells

Molecular and Cellular Biology

Volumn 22, Issue 21, 2002, Pages 7645-7657

  Gu, Yi ^a   Byrne, Michael C ^a   Paranavitana, Nivanka C ^a   Aronow, Bruce ^a   Siefring, Jamie E ^a   D'Souza, Maria ^a   Horton, Heidi F ^a   Quilliam, Lawrence A ^a   Williams, David A ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMASE; GENE PRODUCT; GUANOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN MMCP7; RAC PROTEIN; RAC2 PROTEIN; RHO FACTOR; SERUM RESPONSE FACTOR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MAST CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACID MOTIFS; ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BONE MARROW CELLS; CELL NUCLEUS; DACTINOMYCIN; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAST CELLS; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PLASMIDS; PROTO-ONCOGENE PROTEINS C-KIT; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; STEM CELL FACTOR; TIME FACTORS; TRANSCRIPTION, GENETIC; TRYPTASES; UP-REGULATION;

ANIMALIA;

EID: 0036837891     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.22.21.7645-7657.2002     Document Type: Article

References (76)

1. Alai, M., A. L.-F. Mui, R. L. Cutler, X. R. Bustolo, and M. Barbacid. 1992. Steel factor stimulates the tyrosine phosphorylation of the proto-oncogene product, p95vav, in human hematopoietic cells. J. Biol. Chem. 267:18021-18025.
2. Angel, P., E. A. Allegretto, S. T. Okino, K. Hattori, W. J. Boyle, T. Hunter, and M. Karin. 1988. Oncogene jun encodes a sequence-specific trans-activator similar to AP-1. Nature 332:166-171.
3. Arbibe, L., J. P. Mira, N. Teusch, L. Kline, M. Guha, N. Mackman, P. J. Godowski, R. J. Ulevitch, and U. G. Knaus. 2000. Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat. Immunol. 1:533-540.
4. Baldwin, A. S., Jr. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-683.
5. Benard, V., B. P. Bohl, and G. M. Bokoch. 1999. Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils with a novel assay for active GTPases. J. Biol. Chem. 274:13198-13204.
6. Byrne, M. C., M. Z. Whitley, and M. T. Follettie. 2000. Preparation of mRNA expression monitoring, 4th ed., p. 22.2.1-22.2.13. In F. M. Ausubel (ed.), Current protocols in molecular biology. John Wiley and Sons, Inc., New York, N.Y.
7. Camoretti-Mercado, B., H. W. Liu, A. J. Halayko, S. M. Forsythe, J. W. Kyle, B. Li, Y. Fu, J. McConville, P. Kogut, J. E. Vieira, N. M. Patel, M. B. Hershenson, E. Fuchs, S. Sinha, J. M. Miano, M. S. Parmacek, J. K. Burkhardt, and J. Solway. 2000. Physiological control of smooth muscle-specific gene expression through regulated nuclear translocation of serum response factor. J. Biol. Chem. 275:30387-30393.
8. Coso, O. A., M. Chiariello, J. C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J. S. Gutkind. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137-1146.
9. Crespo, P., X. R. Bustelo, D. S. Aaronson, O. A. Coso, M. Lopez-Barahona, M. Barbacid, and J. S. Gutkind. 1996. Rac-1 dependent stimulation of the JNK/SAPK signaling pathway by Vav. Oncogene 13:455-460.
10. Croker, B. A., D. M. Tarlinton, L. A. Cluse, A. J. Tuxen, A. Light, F. C. Yang, D. A. Williams, and A. W. Roberts. 2002. The Rac2 guanosine triphosphatase regulates B lymphocyte antigen receptor responses and chemotaxis and is required for establishment of B-1a and marginal zone B lymphocytes. J. Immunol. 168:3376-3386.
11. del Pozo, M. A., L. S. Price, N. B. Alderson, X. D. Ren, and M. A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008-2014.
12. De Sanctis, G. T., M. Merchant, D. R. Beier, R. D. Dredge, J. K. Grobholz, T. R. Martin, E. S. Lander, and J. M. Drazen. 1995. Quantitative locus analysis of airway hyperresponsiveness in A/J and C57BL/6J mice. Nat. Genet. 11:150-154.
13. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNKI: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
14. Didsbury, J., R. F. Weber, G. M. Bokosh, T. Evans, and R. Synderman. 1989. Rac, a novel ras-related family of proteins that are botulinum toxin substrates. J. Biol. Chem. 264:16378-16382.
15. Diekmann, D., C. D. Nobes, P. D. Burbelo, A. Abo, and A. Hall. 1995. Rac GTPase interacts with GAPs and target proteins through multiple effector sites. EMBO J. 14:5297-5305.
16. Eklund, K. K., N. Ghildyal, K. F. Austen, and R. L. Stevens. 1993. Induction by IL-9 and suppression by IL-3 and IL-4 of the levels of chromosome 14-derived transcripts that encode late-expressed mouse mast cell proteases. J. Immunol. 151:4266-4273.
17. Ghildyal, N., H. P. McNeil, M. F. Gurish, K. F. Austen, and R. L. Stevens. 1992. Transcriptional regulation of the mucosal mast cell-specific protease gene, MMCP-2, by interleukin 10 and interleukin 3. J. Biol. Chem. 267:8473-8477.
18. Ghildyal, N., H. P. McNeil, S. Stechschulte, K. F. Austen, D. Silberstein, M. F. Gurish, L. L. Somerville, and R. L. Stevens. 1992. IL-10 induces transcription of the gene for mouse mast cell protease-1, a serine protease preferentially expressed in mucosal mast cells of Trichinella spiralis-infected mice. J. Immunol. 149:2123-2129.
19. Ghislain, J. J., and E. N. Fish. 1996. Application of genomic DNA affinity chromatography identifies multiple interferon-alpha-regulated Stat2 complexes. J. Biol. Chem. 271:12408-12413.
20. Gu, Y., B. Jia, F. C. Yang, M. D'Souza, C. E. Harris, C. W. Derrow, Y. Zheng, and D. A. Williams. 2001. Biochemical and biological characterization of a human Rac2 GTPase mutant associated with phagocytic immunodeficiency. J. Biol. Chem. 276:15929-15938.
21. Gurish, M. F., N. Ghildyal, H. P. McNeil, K. F. Austen, S. Gillis, and R. L. Stevens. 1992. Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand. J. Exp Med. 175:1003-1012.
22. Haataja, L., J. Groffen, and N. Heisterkamp. 1997. Characterization of RAC3, a novel member of the Rho family. J. Biol. Chem. 272:20384-20388.
23. Haataja, L., V. Kaartinen, J. Groffen, and N. Heisterkamp. 2002. The small GTPase Rac3 interacts with the integrin-binding protein CIB and promotes integrin alpha(IIb)beta(3)-mediated adhesion and spreading. J. Biol. Chem. 277:8321-8328.
24. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
25. Han, J., K. Luby-Phelps, B. Das, X. Shu, Y. Xia, R. D. Mosteller, U. M. Krishna, J. R. Falck, M. A. White, and D. Broek. 1998. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279:558-560.
26. Hill, C. S., J. Wynne, and R. Treisman. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159-1170.
27. Huang, C., W. Y. Ma, M. R. Young, N. Colburn, and Z. Dong. 1998. Shortage of mitogen-activated protein kinase is responsible for resistance to AP-1 transactivation and transformation in mouse JB6 cells. Proc. Natl. Acad. Sci. USA 95:156-161.
28. Huang, C., G. W. Wong, N. Ghildyal, M. F. Gurish, A. Sali, R. Matsumoto, W. T. Qiu, and R. L. Stevens. 1997. The tryptase, mouse mast cell protease 7, exhibits anticoagulant activity in vivo and in vitro due to its ability to degrade fibrinogen in the presence of the diverse array of protease inhibitors in plasma. J. Biol. Chem. 272:31885-31893.
29. Huang, R. Y., T. Blom, and L. Hellman. 1991. Cloning and structural analysis of MMCP-1, MMCP-4 and MMCP-5, three mouse mast cell-specific serine proteases. Eur. J Immunol. 21:1611-1621.
30. Hunt, J. E., D. S. Friend, M. F. Gurish, E. Feyfant, A. Sali, C. Huang, N. Ghildyal, S. Stechschulte, K. F. Austen, and R. L. Stevens. 1997. Mouse mast cell protease 9, a novel member of the chromosome 14 family of serine proteases that is selectively expressed in uterine mast cells. J. Biol. Chem. 272:29158-29166.
31. Hunt, J. E., R. L. Stevens, K. F. Austen, J. Zhang, Z. Xia, and N. Ghildyal. 1996. Natural disruption of the mouse mast cell protease 7 gene in the C57BL/6 mouse. J. Biol. Chem. 271:2851-2855.
32. Kheradmand, F., E. Werner, P. Tremble, M. Symons, and Z. Werb. 1998. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 280:898-902.
33. Kim, C., and M. C. Dinauer. 2001. Rac2 is an essential regulator of neutrophil nicotinamide adenine dinucleotide phosphate oxidase activation in response to specific signaling pathways. J. Immunol. 166:1223-1232.
34. Kitamura, Y. 1989. Heterogeneity of mast cells and phenotypic change between subpopulations. Annu. Rev. Immunol. 7:59-76.
35. Knaus, U. G., Y. Wang, A. M. Reilly, D. Warnock, and J. H. Jackson. 1998. Structural requirements for PAK activation by Rac GTPases. J. Biol. Chem. 273:21512-21518.
36. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dal, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodett. 1994. The stress-activated protein kinase subfamily of c-jun kinases. Nature 369:156-160.
37. Li, B., H. Yu, W. Zheng, R. Voll, S. Na, A. W. Roberts, D. A. Williams, R. J. Davis, S. Ghosh, and R. A. Flavell. 2000. Role of the guanosine triphosphatase Rac2 in T helper 1 cell differentiation. Science 288:2219-2222.
38. Lutzelschwab, C., M. R. Huang, M. C. Kullberg, M. Aveskogh, and L. Hellman. 1998. Characterization of mouse mast cell protease-8, the first member of a novel subfamily of mouse mast cell serine proteases, distinct from both the classical chymases and tryptases. Eur. J. Immunol. 28:1022-1033.
39. McNeil, H. P., D. S. Reynolds, V. Schiller, N. Ghildyal, D. S. Gurley, K. F. Austen, and R. L. Stevens. 1992. Isolation, characterization, and transcription of the gene encoding mouse mast cell protease 7. Proc. Natl. Acad. Sci. USA 89:11174-11178.
40. Michaelson, D., J. Silletti, G. Murphy, P. D'Eustachio, M. Rush, and M. R. Philips. 2001. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152:111-126.
41. Minden, A., A. Lin, F. X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
42. Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Derijard, R. J. Davis, G. L. Johnson, and M. Karin. 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
43. Miranti, C. K., L. Leng, P. Maschberger, J. S. Brugge, and S. J. Shattil. 1998. Identification of a novel integrin signaling pathway involving the kinase Syk and the guanine nucleotide exchange factor Vav1. Curr. Biol. 8:1289-1299.
44. Moll, J., G. Sansig, E. Fattori, and H. van der Putten. 1991. The murine rac1 gene: cDNA cloning, tissue distribution and regulated expression of rac1 mRNA by disassembly of actin microfilaments. Oncogene. 6:863-866.
45. Nobes, C. D., and A. Hall. 1995. Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
46. Nobes, C. D., P. Hawkins, L. Stephens, and A. Hall. 1995. Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108:225-233.
47. Ogihara, H., E. Morii, D. K. Kim, K. Oboki, and Y. Kitamura. 2001. Inhibitory effect of the transcription factor encoded by the mutant mi microphthalmia allele on transactivation of mouse mast cell protease 7 gene. Blood 97:645-651.
48. 1. Science 269:1270-1272.
49. Pande, A., J. Pande, N. Asherie, A. Lomakin, O. Ogun, J. A. King, N. H. Lubsen, D. Walton, and G. B. Benedek. 2000. Molecular basis of a progressive juvenile-onset hereditary cataract. Proc. Natl. Acad. Sci. USA 97:1993-1998.
50. Pollok, K., J. van der Loo, R. Cooper, L. Kennedy, and D. Williams. 1999. Costimulation of transduced T lymphocytes via T-cell receptor/CD3 complex and CD28 leads to increased transcription of integrated retrovirus. Hum. Gene Ther. 10:2221-2236.
51. Reynolds, D. S., D. S. Gurley, K. F. Austen, and W. E. Serafin. 1991. Cloning of the cDNA and gene of mouse mast cell protease-6. Transcription by progenitor mast cells and mast cells of the connective tissue subclass. J. Biol. Chem. 266:3847-3853.
52. Roberts, A. W., C. Kim, L. Zhen, J. B. Lowe, R. Kapur, B. Petryniak, A. Spaetti, J. D. Pollock, J. B. Borneo, G. B. Bradford, S. J. Atkinson, M. C. Dinauer, and D. A. Williams. 1999. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10:183-196.
53. Sanders, L., F. Matsumura, G. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21-activated kinase. Science 283:2083-2085.
54. Sekizawa, K., G. H. Caughey, S. C. Lazarus, W. M. Gold, and J. A. Nadel. 1989. Mast cell tryptase causes airway smooth muscle hyperresponsiveness in dogs. J. Clin. Investig. 83:175-179.
55. Serafin, W. E., D. S. Reynolds, S. Rogelj, W. S. Lane, G. A. Conder, S. S. Johnson, K. F. Austen, and R. L. Stevens. 1990. Identification and molecular cloning of a novel mouse mucosal mast cell serine protease. J. Biol. Chem. 265:423-429.
56. Serafin, W. E., T. P. Sullivan, G. A. Conder, A. Ebrahimi, P. Marcham, S. S. Johnson, K. F. Austen, and D. S. Reynolds. 1991. Cloning of the cDNA and gene for mouse mast cell protease 4. Demonstration of its late transcription in mast cell subclasses and analysis of its homology to subclass-specific neutral proteases of the mouse and rat. J. Biol. Chem. 266:1934-1941.
57. Shirsat, N. V., R. J. Pignolo, B. L. Kreider, and G. Rovera. 1990. A member of the ras gene superfamily is expressed specifically in T, B and myeloid hemopoietic cells. Oncogene 5:769-772.
58. Spiegelman, B. M., M. Frank, and H. Green. 1983. Molecular cloning of mRNA from 3T3 adipocytes. Regulation of mRNA content for glycerophosphate dehydrogenase and other differentiation-dependent proteins during adipocyte development. J. Biol. Chem. 258:10083-10089.
59. Sulciner, D. J., K. Irani, Z. X. Yu, V. J. Ferrans, P. Goldschmidt-Clermont, and T. Finkel. 1996. rac1 regulates a cytokine-stimulated, redox-dependent pathway necessary for NF-κB activation Mol. Cell. Biol. 16:7115-7121.
60. Symons, M., and J. Settleman. 2000. Rho family GTPases: more than simple switches. Trends Cell Biol. 10:415-419.
61. Thomas, P. S. 1980. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77:5201-5205.
62. Timokhina, I., H. Kissel, G. Stella, and P. Besmer. 1998. Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J. 17:6250-6262.
63. Tsujimura, T., U. Koshimizu, H. Katoh, K. Isozaki, Y. Kanakura, T. Tono, S. Adachi, T. Kasugai, H. Tei, Y. Nishimune, et al. 1993. Mast cell number in the skin of heterozygotes reflects the molecular nature of c-kit mutation. Blood 81:2530-2538.
64. Uddin, S., E. N. Fish, D. Sher, C. Gardziola, O. R. Colamonici, M. Kellum, P. M. Pitha, M. F. White, and L. C. Platanias. 1997. The IRS-pathway operates distinctively from the Stat-pathway in hematopoietic cells and transduces common and distinct signals during engagement of the insulin or interferon-alpha receptors. Blood 90:2574-2582.
65. Uddin, S., F. Lekmine, N. Sharma, B. Majchrzak, I. Mayer, P. R. Young, G. M. Bokoch, E. N. Fish, and L. C. Platanias. 2000. The Rac1/p38 mitogen-activated protein kinase pathway is required for interferon alpha-dependent transcriptional activation but not serine phosphorylation of Stat proteins. J. Biol. Chem. 275:27634-27640.
66. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
67. van Oers, N. S., W. Tao, J. D. Watts, P. Johnson, R. Aebersold, and H. S. Teh. 1993. Constitutive tyrosine phosphorylation of the T-cell receptor (TCR) zeta subunit: regulation of TCR-associated protein tyrosine kinase activity by TCR zeta. Mol. Cell. Biol. 13:5771-5780.
68. Vojtek, A. B., and J. A. Cooper. 1995. Rho family members: activators of MAP kinase cascades. Cell 82:527-529.
69. Vosseller, K., G. Stella, N. S. Yee, and P. Besmer. 1997. c-Kit receptor signaling through its phosphatidylinositide-3′-kinase-binding site and protein kinase C: role in mast cell enhancement of degranulation, adhesion, and membrane ruffling. Mol. Biol. Cell 8:909-922.
70. Westwick, J. K., Q. T. Lambert, G. J. Clark, M. Symons, L. Van Aelst, R. G. Pestell, and C. J. Der. 1997. Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Mol. Cell Biol. 17:1324-1335.
71. Williams, D. A., W. Tao, F. C. Yang, C. Kim, Y. Gu, P. Mansfield, J. E. Levine, B. Petryniak, C. W. Derrrow, C. Harris, B. Jia, Y. Zheng, D. R. Ambruso, J. B. Lowe, S. J. Atkinson, M. C. Dinauer, and L. Boxer. 2000. A dominant negative mutation of the hematopoiesis-specific RhoGTPase, Rac 2, is associated with a human phagocyte immunodeficiency. Blood 96:1646-1654.
72. Wong, G. W., Y. Tang, E. Feyfant, A. Sali, L. Li, Y. Li, C. Huang, D. S. Friend, S. A. Krilis, and R. L. Stevens. 1999. Identification of a new member of the tryptase family of mouse and human mast cell proteases which possesses a novel COOH-terminal hydrophobic extension. J. Biol. Chem. 274:30784-30793.
73. Xia, Z., N. Ghildyal, K. F. Austen, and R. L. Stevens. 1996. Posttranscriptional regulation of chymase expression in mast cells. A cytokine-dependent mechanism for controlling the expression of granule neutral proteases of hematopoietic cells. J. Biol. Chem. 271:8747-8753.
74. Yang, F. C., S. J. Atkinson, Y. Gu, J. B. Borneo, A. W. Roberts, Y. Zheng, J. Pennington, and D. A. Williams. 2001. Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc. Natl. Acad. Sci. USA 98:5614-5618.
75. L expression while mediating survival and actin-based cell functions in primary mast cells. Immunity 12:557-568.
76. Zheng, Y. 2001. Dbl family guanine nucleotide exchange factors. Trends Biochem. Sci. 26:724-732.