Noncanonical Gβ Gib2 is a scaffolding protein promoting camp signaling through functions of ras1 and cac1 proteins in cryptococcus neoformans

Journal of Biological Chemistry

Volumn 289, Issue 18, 2014, Pages 12202-12216

  Wang, Yanli ^a,g   Shen, Gui ^a   Gong, Jinjun ^a   Shen, Danyu ^b   Whittington, Amy ^c,h   Qing, Jiang ^a   Treloar, Joshua ^e   Boisvert, Scott ^f   Zhang, Zhengguang ^b   Yang, Cai ^a   Wang, Ping ^a,c,d  

^a CHILDREN S HOSPITAL   (United States)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

^c Departments of Microbiology Immunology and Parasitology   (China)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Tulane University   (United States)

^f Duke University   (United States)

^g INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^h UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

ADAPTOR PROTEINS; CRYPTOCOCCUS NEOFORMANS; KEY ELEMENTS; OVER-EXPRESSION; REGULATORY NETWORK; SCAFFOLDING PROTEINS;

SCAFFOLDS (BIOLOGY);

ADAPTOR PROTEIN; ADENYLATE CYCLASE; CYCLIC AMP; FUNGAL PROTEIN; GLUTATHIONE TRANSFERASE; GUANOSINE TRIPHOSPHATASE; PROTEIN CAC1; PROTEIN GIB2; PROTEIN GPA1; PROTEIN RAS1; REGULATOR PROTEIN; SCAFFOLD PROTEIN; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CAC1 GENE; CELL FUNCTION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; ENERGY YIELD; ENZYME ACTIVITY; FUNGAL GENE; FUNGAL METABOLISM; FUNGAL VIRULENCE; FUNGUS GROWTH; GPA1 GENE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RAS1 GENE; RIBOSOME; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE (ADENYLYL CYCLASE); CYCLIC AMP (CAMP); FUNGAL GROWTH AND VIRULENCE; G PROTEINS; GΒ-LIKE/RACK1; PROTEIN INTERACTIVE NETWORK; RAS; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CRYPTOCOCCUS NEOFORMANS; CYCLIC AMP; FUNGAL PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PROTEIN BINDING; PROTEIN INTERACTION MAPS; RAS PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84899728598     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537183     Document Type: Article

References (62)

1. Park, B. J., Wannemuehler, K. A., Marston, B. J., Govender, N., Pappas, P. G., and Chiller, T. M. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23, 525-530
2. Kozel, T. R. (1995) Virulence factors of Cryptococcus neoformans. Trends Microbiol. 3, 295-299
3. Buchanan, K. L., and Murphy, J. W. (1998) What makes Cryptococcus neoformans a pathogen? Emerg. Infect. Dis. 4, 71-83
4. Lengeler, K. B., Davidson, R. C., D'souza, C., Harashima, T., Shen, W.-C., Wang, P., Pan, X., Waugh, M., and Heitman, J. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64, 746-785
5. Kays, A. M., and Borkovich, K. A. (2004) Signal Transduction Pathways Mediated by Heterotrimeric G Proteins, pp. 175-207, Springer-Verlag, Berlin and Heidelberg
6. Hoffman, C. S. (2005) Except in every detail: comparing and contrasting G-protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eukaryot. Cell 4, 495-503
7. Gilman, A. G. (1987) G-proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649
8. Alspaugh, J. A., Perfect, J. R., and Heitman, J. (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein subunit GPA1 and cAMP. Genes Dev. 11, 3206-3217
9. Wang, P., Perfect, J. R., and Heitman, J. (2000) The G-protein subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell. Biol. 20, 352-362
10. Hsueh, Y. P., Xue, C., and Heitman, J. (2007)Gprotein signaling governing cell fate decisions involves opposing G subunits in Cryptococcus neoformans. Mol. Biol. Cell 18, 3237-3249
11. Li, L., Shen, G., Zhang, Z. G., Wang, Y. L., Thompson, J. K., and Wang, P. (2007) Canonical heterotrimeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol. Biol. Cell 18, 4201-4209
12. Xue, C., Bahn, Y. S., Cox, G. M., and Heitman, J. (2006) G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol. Biol. Cell 17, 667-679
13. Alspaugh, J. A., Pukkila-Worley, R., Harashima, T., Cavallo, L. M., Funnell, D., Cox, G. M., Perfect, J. R., Kronstad, J. W., and Heitman, J. (2002) Adenylyl cyclase functions downstream of the G protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot. Cell 1, 75-84
14. D'Souza, C. A., Alspaugh, J. A., Yue, C., Harashima, T., Cox, G. M., Perfect, J. R., and Heitman, J. (2001) Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol. Cell. Biol. 21, 3179-3191
15. Hicks, J. K., Bahn, Y. S., and Heitman, J. (2005) Pde1 phosphodiesterase modulates cyclic AMP levels through a protein kinase A-mediated negative feedback loop in Cryptococcus neoformans. Eukaryot. Cell 4, 1971-1981
16. Waugh, M. S., Nichols, C. B., DeCesare, C. M., Cox, G. M., Heitman, J., and Alspaugh, J. A. (2002) Ras1 and Ras2 contribute shared and unique roles in physiology and virulence of Cryptococcus neoformans. Microbiology 148, 191-201
17. Palmer, D. A., Thompson, J. K., Li, L., Prat, A., and Wang, P. (2006) Gib2, a novel G-like/RACK1 homolog, functions as a G subunit in cAMP signaling and is essential in Cryptococcus neoformans. J. Biol. Chem. 281, 32596-32605
18. Guillemot, F., Billault, A., and Auffray, C. (1989) Physical linkage of a guanine nucleotide-binding protein-related gene to the chicken major histocompatibility complex. Proc. Natl. Acad. Sci. U.S.A. 86, 4594-4598
19. Ron, D., Chen, C. H., Caldwell, J., Jamieson, L., Orr, E., and Mochly-Rosen, D. (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the subunit of G proteins. Proc. Natl. Acad. Sci. U.S.A. 91, 839-843
20. Ron, D., Jiang, Z., Yao, L., Vagts, A., Diamond, I., and Gordon, A. (1999) Coordinated movement of RACK1 with activated-IIPKC. J. Biol. Chem. 274, 27039-27046
21. Liliental, J., and Chang, D. D. (1998) Rack1, a receptor for activated protein kinase C, interacts with integrin subunit. J. Biol. Chem. 273, 2379-2383
22. Chang, B. Y., Conroy, K. B., Machleder, E. M., and Cartwright, C. A. (1998) RACK1, a receptor for activated C kinase and a homolog of the subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18, 3245-3256
23. Chang, B. Y., Harte, R. A., and Cartwright, C. A. (2002) RACK1: a novel substrate for the Src protein-tyrosine kinase. Oncogene 21, 7619-7629
24. Dell, E. J., Connor, J., Chen, S., Stebbins, E. G., Skiba, N. P., Mochly-Rosen, D., and Hamm, H. E. (2002) The+ subunit of heterotrimeric G proteins interacts with RACK1 and two other WD repeat proteins. J. Biol. Chem. 277, 49888-49895
25. Chen, S., Dell, E. J., Lin, F., Sai, J., and Hamm, H. E. (2004)RACK1regulates specific functions of G+. J. Biol. Chem. 279, 17861-17868
26. Chen, S., Lin, F., and Hamm, H. E. (2005) RACK1 binds to a signal transfer region of G+ and inhibits phospholipase C+2 activation. J. Biol. Chem. 280, 33445-33452
27. Yarwood, S. J., Steele, M. R., Scotland, G., Houslay, M. D., and Bolger, G. B. (1999) The RACK1 signaling scaffold protein selectively interacts with the cAMP-specific phosphodiesterase PDE4D5 isoform. J. Biol. Chem. 274, 14909-14917
28. Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L. A., Offenhäuser, N., Marchisio, P. C., and Biffo, S. (2003) Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426, 579-584
29. Nilsson, J., Sengupta, J., Frank, J., and Nissen, P. (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep. 5, 1137-1141
30. Zeller, C. E., Parnell, S. C., and Dohlman, H. G. (2007) The RACK1 ortholog Asc1 functions as a G-protein subunit coupled to glucose responsiveness in yeast. J. Biol. Chem. 282, 25168-25176
31. Gerbasi, V. R., Weaver, C. M., Hill, S., Friedman, D. B., and Link, A. J. (2004) Yeast Asc1p and mammalian RACK1 are functionally orthologous core 40S ribosomal proteins that repress gene expression. Mol. Cell. Biol. 24, 8276-8287
32. Valerius, O., Kleinschmidt, M., Rachfall, N., Schulze, F., López Marín, S., Hoppert, M., Streckfuss-Bömeke, K., Fischer, C., and Braus, G. H. (2007) The Saccharomyces homolog of mammalian RACK1, Cpc2/Asc1p, is required for FLO11-dependent adhesive growth and dimorphism. Mol. Cell. Proteomics 6, 1968-1979
33. McLeod, M., Shor, B., Caporaso, A., Wang, W., Chen, H., and Hu, L. (2000) Cpc2, a fission yeast homologue of mammalian RACK1 protein, interacts with Ran1 (Pat1) kinase to regulate cell cycle progression and meiotic development. Mol. Cell. Biol. 20, 4016-4027
34. Wang, L., Berndt, P., Xia, X., Kahnt, J., and Kahmann, R. (2011) A seven- WD40protein related to human RACK1 regulates mating and virulence in Ustilago maydis. Mol. Microbiol. 81, 1484-1498
35. Kwon-Chung, K. J., Edman, J. C., and Wickes, B. L. (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 60, 602-605
36. Perfect, J. R., Toffaletti, D. L., and Rude, T. H. (1993) The gene encoding phosphoribosylaminoimidazole carboxylase (ADE2) is essential for growth of Cryptococcus neoformans in cerebrospinal fluid. Infect. Immun. 61, 4446-4451
37. Wang, P., Cutler, J., King, J., and Palmer, D. (2004) Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryot. Cell 3, 1028-1035
38. Sambrook, J., and Russell, D. G. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 39. Shen, G., Whittington, A., Song, K., and Wang, P. (2010) Pleiotropic function of intersectin homologue Cin1 in Cryptococcus neoformans. Mol. Microbiol. 76, 662-676
39. Edman, J. C. (1992) Isolation of telomerelike sequences from Cryptococcus neoformans and their use in high-efficiency transformation. Mol. Cell. Biol. 12, 2777-2783
40. McDade, H. C., and Cox, G. M. (2001) A new dominant selectable marker for use in Cryptococcus neoformans. Med. Mycol. 39, 151-154
41. Wang, P., Cox, G. M., and Heitman, J. (2004) A Sch9 protein kinase homologue controlling virulence independently of the cAMP pathway in Cryptococcus neoformans. Curr. Genet. 46, 247-255
42. James, P., Halladay, J., and Craig, E. A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436
43. Qian, J., Cole, R. B., and Cai, Y. (2011) Synthesis and characterization of a 'fluorous' (fluorinated alkyl) affinity reagent that labels primary amine groups in proteins/peptides. J. Mass Spectrom. 46, 1-11
44. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8- A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
45. Dolinski, K., Muir, S., Cardenas, M., and Heitman, J. (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94, 13093-13098
46. Bolger, G. B., McCahill, A., Yarwood, S. J., Steele, M. R., Warwicker, J., and Houslay, M. D. (2002) Delineation of RAID1, the RACK1 interaction domain located within the unique N-terminal region of the cAMP-specific phosphodiesterase, PDE4D5. BMC Biochem. 3, 24
47. Davidson, R. C., Blankenship, J. R., Kraus, P. R., de Jesus Berrios, M., Hull, C. M., D'Souza, C., Wang, P., and Heitman, J. (2002)APCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148, 2607-2615
48. Shen, G., Wang, Y. L., Whittington, A., Li, L., and Wang, P. (2008) The RGS protein Crg2 regulates pheromone and cyclicAMPsignaling in Cryptococcus neoformans. Eukaryot. Cell 7, 1540-1548
49. Kataoka, T., Broek, D., and Wigler, M. (1985) DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell 43, 493-505
50. Toda, T., Uno, I., Ishikawa, T., Powers, S., Kataoka, T., Broek, D., Cameron, S., Broach, J., Matsumoto, K., and Wigler, M. (1985) In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40, 27-36
51. Mintzer, K. A., and Field, J. (1994) Interactions between adenylyl cyclase, CAP and RAS from Saccharomyces cerevisiae. Cell. Signal. 6, 681-694
52. Kido, M., Shima, F., Satoh, T., Asato, T., Kariya, K., and Kataoka, T. (2002) Critical function of the Ras-associating domain as a primary Ras-binding site for regulation of Saccharomyces cerevisiae adenylyl cyclase. J. Biol. Chem. 277, 3117-3123
53. Alspaugh, J. A., Cavallo, L. M., Perfect, J. R., and Heitman, J. (2000) RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol. Microbiol. 36, 352-365
54. Shen, G., Zhou, E., Alspaugh, J. A., and Wang, P. (2012) Wsp1 is downstream of Cin1 and regulates vesicle transport and actin cytoskeleton as an effector of Cdc42 and Rac1 in Cryptococcus neoformans. Eukaryot. Cell 11, 471-481
55. Adams, D. R., Ron, D., and Kiely, P. A. (2011) RACK1, A multifaceted scaffolding protein: structure and function. Cell Commun. Signal. 9, 22
56. Marcotte, E. M., Pellegrini, M., Thompson, M. J., Yeates, T. O., and Eisenberg, D. (1999) A combined algorithm for genome-wide prediction of protein function. Nature 402, 83-86
57. Mohseni-Zadeh, S., Camonis, J., Wojcik, J., and Barillot, E. (2004) in Genome Informatics 2004, Presented at the 15th International Conference on Genome InformaticsDecember 16-18, 2004, Yokohama Pacifico, Japan, Abstr. P120, Japanese Society for Bioinformatics, Tokyo
58. Linder, P., and Slonimski, P. P. (1989) An essential yeast protein, encoded by duplicated genes TIF1 and TIF2 and homologous to the mammalian translation initiation factor eIF-4A, can suppress a mitochondrial missense mutation. Proc. Natl. Acad. Sci. U.S.A. 86, 2286-2290
59. Cramer, K. L., Gerrald, Q. D., Nichols, C. B., Price, M. S., and Alspaugh, J. A. (2006) Transcription factor Nrg1 mediates capsule formation, stress response, and pathogenesis in Cryptococcus neoformans. Eukaryot. Cell 5, 1147-1156
60. Mudge, D. K., Yang, F., Currie, B. M., Kim, J. M., Yeda, K., Bashyakarla, V. K., Ivey, F. D., and Hoffman, C. S. (2014) Sck1 negatively-regulates Gpa2-mediated glucose signaling in Schizosaccharomyces pombe. Eukaryot. Cell 13, 202-208
61. Tolkacheva, T., McNamara, P., Piekarz, E., and Courchesne, W. (1994) Cloning of a Cryptococcus neoformans gene, GPA1, encoding a G-protein-subunit homolog. Infect. Immun. 62, 2849-2856
62. Xue, C., Hsueh, Y. P., Chen, L., and Heitman, J. (2008) The RGS protein Crg2 regulates both pheromone and cAMP signalling in Cryptococcus neoformans. Mol. Microbiol. 70, 379-395