Ectopic expression of cyclase associated protein CAP restores the streaming and aggregation defects of adenylyl cyclase a deficient Dictyostelium discoideum cells

BMC Developmental Biology

Volumn 12, Issue , 2012, Pages

  Sultana, Hameeda ^a,b   Neelakanta, Girish ^b   Rivero, Francisco ^c   Blau Wasser, Rosemarie ^a   Schleicher, Michael ^d   Noegel, Angelika A ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HULL   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Adenylyl cyclase ACA; Adenylyl cyclase ACB; aggregation; Cell polarity; cell adhesion; Cyclase associated protein; development

Indexed keywords

ANIMALIA; DICTYOSTELIUM DISCOIDEUM; MAMMALIA;

ADENYLATE CYCLASE; CYTOSKELETON PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTOZOAL PROTEIN;

ARTICLE; BIOSYNTHESIS; CELL ADHESION; CELL POLARITY; CYTOLOGY; DICTYOSTELIUM; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ADENYLATE CYCLASE; CELL ADHESION; CELL POLARITY; CYTOSKELETAL PROTEINS; DICTYOSTELIUM; GREEN FLUORESCENT PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84855602780     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-12-3     Document Type: Article

References (48)

1. Cell aggregation and differentiation in Dictyostelium. Gerisch G, Curr Top Dev Biol 1968 3 157 197 5002049
2. Follow the leader. Meili R, Firtel RA, Dev Cell 2003 4 291 293 10.1016/S1534-5807(03)00064-9 12636911 (Pubitemid 36342355)
3. Cell-cell adhesion and morphogenesis in Dictyostelium discoideum. Siu CH, Kamboj RK, Dev Genet 1990 11 377 387 10.1002/dvg.1020110509 2096015
4. Dictyostelium: a model for regulated cell movement during morphogenesis. Firtel RA, Meili R, Curr Opin Genet Dev 2000 10 421 427 10.1016/S0959-437X(00) 00107-6 10889066 (Pubitemid 30450047)
5. Cell-cell adhesion and signal transduction during Dictyostelium development. Coates JC, Harwood AJ, J Cell Sci 2001 114 4349 4358 11792801 (Pubitemid 34082856)
6. Constitutive overexpression of the contact site A glycoprotein enables growth-phase cells of Dictyostelium discoideum to aggregate. Faix J, Gerisch G, Noegel AA, Embo J 1990 9 2709 2716 2390970
7. Characterization of the cell adhesion molecule gp24 in Dictyostelium discoideum. Mediation of cell-cell adhesion via a Ca(2+)-dependent mechanism. Brar SK, Siu CH, J Biol Chem 1993 268 24902 24909 8227052
8. Molecular cloning and characterization of DdCAD-1, a Ca2+-dependent cell-cell adhesion molecule, in Dictyostelium discoideum. Wong EF, Brar SK, Sesaki H, Yang C, Siu CH, J Biol Chem 1996 271 16399 16408 10.1074/jbc.271.27. 16399 8663243 (Pubitemid 26236266)
9. Involvement of cell-cell adhesion in the expression of the cell cohesion molecule gp80 in Dictyostelium discoideum. Desbarats L, Brar SK, Siu CH, J Cell Sci 1994 107 1705 1712 7962211 (Pubitemid 24198489)
10. The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. Wang J, Hou L, Awrey D, Loomis WF, Firtel RA, Siu CH, Dev Biol 2000 227 734 745 10.1006/dbio.2000.9881 11071787
11. Molecular genetics of signal transduction in Dictyostelium. Parent CA, Devreotes PN, Annu Rev Biochem 1996 65 411 440 10.1146/annurev.bi.65.070196. 002211 8811185 (Pubitemid 26250615)
12. Group migration and signal relay in Dictyostelium. Kriebel PW, Parent CA, Methods Mol Biol 2009 571 111 124 10.1007/978-1-60761-198-1-7 19763962
13. cAMP signaling in Dictyostelium. Complexity of cAMP synthesis, degradation and detection. Saran S, Meima ME, Alvarez-Curto E, Weening KE, Rozen DE, Schaap P, J Muscle Res Cell Motil 2002 23 793 802 10.1023/A:1024483829878 12952077 (Pubitemid 36995058)
14. Adenylyl cyclase localization regulates streaming during chemotaxis. Kriebel PW, Barr VA, Parent CA, Cell 2003 112 549 560 10.1016/S0092-8674(03) 00081-3 12600317 (Pubitemid 36263086)
15. Cell polarity and Dictyostelium development. Williams HP, Harwood AJ, Curr Opin Microbiol 2003 6 621 627 10.1016/j.mib.2003.10.008 14662359 (Pubitemid 38020060)
16. Identification of a cyclase-associated protein (CAP) homologue in Dictyostelium discoideum and characterization of its interaction with actin. Gottwald U, Brokamp R, Karakesisoglou I, Schleicher M, Noegel AA, Mol Biol Cell 1996 7 261 272 8688557 (Pubitemid 26064371)
17. Assessing the role of the ASP56/CAP homologue of Dictyostelium discoideum and the requirements for subcellular localization. Noegel AA, Rivero F, Albrecht R, Janssen KP, Köhler J, Parent CA, Schleicher M, J Cell Sci 1999 112 3195 3203 10504325 (Pubitemid 29507200)
18. The cyclase-associated protein CAP as regulator of cell polarity and cAMP signaling in Dictyostelium. Noegel AA, Blau-Wasser R, Sultana H, Müller R, Israel L, Schleicher M, Patel H, Weijer CJ, Mol Biol Cell 2004 15 934 945 14595119 (Pubitemid 38146505)
19. Microarray phenotyping places cyclase associated protein CAP at the crossroad of signaling pathways reorganizing the actin cytoskeleton in Dictyostelium. Sultana H, Neelakanta G, Eichinger L, Rivero F, Noegel AA, Exp Cell Res 2009 315 127 140 10.1016/j.yexcr.2008.10.023 19010323
20. Coiled-coil interaction of N-terminal 36 residues of cyclase-associated protein with adenylyl cyclase is sufficient for its function in Saccharomyces cerevisiae ras pathway. Nishida Y, Shima F, Sen H, Tanaka Y, Yanagihara C, Yamawaki-Kataoka Y, Kariya K, Kataoka T, J Biol Chem 1998 273 28019 28024 10.1074/jbc.273.43.28019 9774417 (Pubitemid 28496094)
21. Phosphorylation of the Dictyostelium myosin II heavy chain is necessary for maintaining cellular polarity and suppressing turning during chemotaxis. Stites J, Wessels D, Uhl A, Egelhoff T, Shutt D, Soll DR, Cell Motil Cytoskeleton 1998 39 31 51 10.1002/(SICI)1097-0169(1998)39:1<31::AID- CM4>3.0.CO;2-J 9453712 (Pubitemid 28042457)
22. Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Pitt GS, Milona N, Borleis J, Lin KC, Reed RR, Devreotes PN, Cell 1992 69 305 315 10.1016/0092-8674(92)90411-5 1348970
23. Complete sequence and transcript regulation of a cell adhesion protein from aggregating Dictyostelium cells. Noegel A, Gerisch G, Stadler J, Westphal M, EMBO J 1986 5 1473 1476 16453689
24. Extracellular cAMP is sufficient to restore developmental gene expression and morphogenesis in Dictyostelium cells lacking the aggregation adenylyl cyclase (ACA). Pitt GS, Brandt R, Lin KC, Devreotes PN, Schaap P, Genes Dev 1993 7 2172 2180 10.1101/gad.7.11.2172 8224844 (Pubitemid 23336143)
25. A conserved proline-rich region of the Saccharomyces cerevisiae cyclase-associated protein binds SH3 domains and modulates cytoskeletal localization. Freeman NL, Lila T, Mintzer KA, Chen Z, Pahk AJ, Ren R, Drubin DG, Field J, Mol Cell Biol 1996 16 548 556 8552082
26. A cytoskeletal localizing domain in the cyclase-associated protein, CAP/Srv2p, regulates access to a distant SH3-binding site. Yu J, Wang C, Palmieri SJ, Haarer BK, Field J, J Biol Chem 1999 274 19985 19991 10.1074/jbc.274.28.19985 10391948 (Pubitemid 29327786)
27. Dictyostelium development in the absence of cAMP. Wang B, Kuspa A, Science 1997 277 251 254 10.1126/science.277.5323.251 9211856 (Pubitemid 27446083)
28. Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum. Iranfar N, Fuller D, Loomis WF, Eukaryot Cell 2003 2 664 670 10.1128/EC.2.4.664-670.2003 12912885 (Pubitemid 36996712)
29. Expression of Y53A-actin in Dictyostelium disrupts the cytoskeleton and inhibits intracellular and intercellular chemotactic signaling. Shu S, Liu X, Kriebel PW, Hong MS, Daniels MP, Parent CA, Korn ED, J Biol Chem 2010 285 27713 27725 10.1074/jbc.M110.116277 20610381
30. Actin crosslinking proteins, cortexillin I and II, are required for cAMPsignaling during Dictyostelium chemotaxis and development. Shu S, Liu X, Kriebel PW, Daniels MP, Korn ED, Mol Biol Cell
31. Arabidopsis CAP1-a key regulator of actin organisation and development. Deeks MJ, Rodrigues C, Dimmock S, Ketelaar T, Maciver SK, Malhá R, Hussey PJ, J Cell Sci 2007 120 2609 2618 10.1242/jcs.007302 17635992 (Pubitemid 47323869)
32. Signaling pathways controlling cell polarity and chemotaxis. Chung CY, Funamoto S, Firtel RA, Trends Biochem Sci 2001 26 557 566 10.1016/S0968-0004(01) 01934-X 11551793 (Pubitemid 32823441)
33. Role of cyclic GMP in signal transduction to cytoskeletal myosin. Liu G, Newell PC, Symp Soc Exp Biol 1993 47 283 295 8165571
34. Cyclase-associated proteins: CAPacity for linking signal transduction and actin polymerization. Hubberstey AV, Mottillo EP, Faseb J 2002 16 487 499 10.1096/fj.01-0659rev 11919151 (Pubitemid 34273232)
35. Differentiation and gene regulation. A rich developmental stew. Firtel RA, Ish-Horowicz D, Curr Opin Genet Dev 2000 10 469 470 10.1016/S0959-437X(00) 00114-3 10980422
36. Regulation of cell-cell adhesion during Dictyostelium development. Siu CH, Harris TJ, Wang J, Wong E, Semin Cell Dev Biol 2004 15 633 641 15561583 (Pubitemid 39550243)
37. Two-phase regulatory pathway controls cAMP receptor-mediated expression of early genes in Dictyostelium. Mann SK, Firtel RA, Proc Natl Acad Sci USA 1989 86 1924 1928 10.1073/pnas.86.6.1924 2538821
38. Overexpression of the csA cell adhesion molecule under its own cAMP-regulated promoter impairs morphogenesis in Dictyostelium. Faix J, Gerisch G, Noegel AA, J Cell Sci 1992 102 203 214 1328260
39. Regulation of slug size by the cell adhesion molecule gp80 in Dictyostelium discoideum. Kamboj RK, Lam TY, Siu CH, Cell Regul 1990 1 715 729 1966011
40. Cell polarity and Dictyostelium development. Williams HP, Harwood AJ, Curr Opin Microbiol 2003 6 621 627 10.1016/j.mib.2003.10.008 14662359 (Pubitemid 38020060)
41. Cyclase-associated protein is essential for the functioning of the endo-lysosomal system and provides a link to the actin cytoskeleton. Sultana H, Rivero F, Blau-Wasser R, Schwager S, Balbo A, Bozzaro S, Schleicher M, Noegel AA, Traffic 2005 6 930 946 10.1111/j.1600-0854.2005.00330.x 16138906 (Pubitemid 41309401)
42. Carbohydrate and other epitopes of the contact site A glycoprotein of Dictyostelium discoideum as characterized by monoclonal antibodies. Berthold G, Stadler J, Bozzaro S, Fichtner B, Gerisch G, Cell Differ 1985 16 187 202 2408765 (Pubitemid 15032990)
43. Localization of two phosphorylation sites adjacent to a region important for polymerization on the tail of Dictyostelium myosin. Pagh K, Maruta H, Claviez M, Gerisch G, EMBO J 1984 3 3271 3278 16453592
44. New actin-binding proteins from Dictyostelium discoideum. Schleicher M, Gerisch G, Isenberg G, EMBO J 1984 3 2095 2100 16453551
45. Monoclonal antibodies prepared against Dictyostelium actin: characterization and interactions with actin. Simpson PA, Spudich JA, Parham P, J Cell Biol 1984 99 287 295 10.1083/jcb.99.1.287 6203918 (Pubitemid 14096892)
46. Loss of the F-actin binding and vesicle associated protein comitin leads to a phagocytosis defect. Schreiner T, Mohrs MR, Blau-Wasser R, von Krempelhuber A, Steinert M, Schleicher M, Noegel AA, Euk Cell 2002 1 906 914 10.1128/EC.1.6.906-914.2002 (Pubitemid 36557711)
47. Assaying cell-cell adhesion. Bozzaro S, Methods Mol Biol 2006 346 449 467 16957307
48. The in vivo role of annexin VII (synexin): characterization of an annexin VII-deficient Dictyostelium mutant indicates an involvement in Ca(2+)-regulated processes. Döring V, Veretout F, Albrecht R, Mühlbauer B, Schlatterer C, Schleicher M, Noegel AA, J Cell Sci 1995 108 2065 2076 7657724