Aldolase sequesters WASP and affects WASP/Arp2/3-stimulated actin dynamics

Journal of Cellular Biochemistry

Volumn 114, Issue 8, 2013, Pages 1928-1939

  Lew, Carolyn Ritterson ^a   Tolan, Dean R ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b Boston University   (United States)

Author keywords

GLYCOLYTIC ENZYME; LAMELLIPODIA; MOONLIGHTING; RNAi

Indexed keywords

ACTIN; ENZYME VARIANT; FRUCTOSE BISPHOSPHATE ALDOLASE; WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CATALYSIS; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CONTROLLED STUDY; DYNAMICS; ENZYME DEFECT; ENZYME INHIBITION; GENE SILENCING; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; STIMULATION;

ACTIN-RELATED PROTEIN 3; ACTINS; ANGIOPOIETINS; ANIMALS; CELL MOVEMENT; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE KNOCKDOWN TECHNIQUES; MICE; NIH 3T3 CELLS; RABBITS; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 84879130009     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24538     Document Type: Article

References (50)

1. Baron CB, Ozaki S, Watanabe Y, Hirata M, LaBelle EF, Coburn RF. 1995. Inositol 1,4,5-trisphosphate binding to porcine tracheal smooth muscle aldolase. J Biol Chem 270:20459-20465.
2. Beernink PT, Tolan DR. 1992. Construction of a high-copy gATG vectorh for expression in Escherichia coli. Protein Expression Purif 3:332-336.
3. Benziane B, Demaretz S, Defontaine N, Zaarour N, Cheval L, Bourgeois S, Klein C, Froissart M, Blanchard A, Paillard M, Gamba G, Houillier P, Laghmani K. 2007. NKCC2 surface expression in mammalian cells: down-regulation by novel interaction with aldolase B. J Biol Chem 282:33817-33830.
4. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
5. Brooks DE. 1976. Activity and androgenic control of glycolytic enzymes in the epididymis and epididymal spermatozoa of the rat. Biochem J 156:527-537.
6. Buscaglia CA, Coppens I, Hol WG, Nussenzweig V. 2003. Sites of interaction between aldolase and thrombospondin-related anonymous protein in plasmodium. Mol Biol Cell 14:4947-4957.
7. Buscaglia CA, Penesetti D, Tao M, Nussenzweig V. 2006. Characterization of an aldolase-binding site in the Wiskott.Aldrich syndrome protein. J Biol Chem 281:1324-1331.
8. Cai L, Makhov AM, Schafer DA, Bear JE. 2008. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134:828-842.
9. Fukuoka M, Miki H, Takenawa T. 1997. Identification of N-WASP homologs in human and rat brain. Gene 196:43-48.
10. Gutman I, Wahlefeld AW. 1983. Metabolites 1. Carbohydrates. In: Bergmeyer HU, Bergmeyer J, Grassl M, editors. Methods of enzymatic analysis. Deerfield Beach, FL: Verlag Chemie. pp 1464-1468.
11. Higgs HN, Blanchoin L, Pollard TD. 1999. Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38:15212-15222.
12. Higgs HN, Pollard TD. 2001. Regulation of actin filament network formation through ARP2/3 complex: Activation by a diverse array of proteins. Annu Rev Biochem 70:649-676.
13. Ishida A, Tada Y, Nimura T, Sueyoshi N, Katoh T, Takeuchi M, Fujisawa H, Taniguchi T, Kameshita I. 2005. Identification of major Ca2t/calmodulindependent protein kinase phosphatase-binding proteins in brain: Biochemical analysis of the interaction. Arch Biochem Biophys 435:134-146.
14. Jewett TJ, Sibley LD. 2003. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in Apicomplexan parasites. Mol Cell 11:885-894.
15. Jimenez C, Portela RA, Mellado M, Rodriguez-Frade JM, Collard J, Serrano A, Martinez AC, Avila J, Carrera AC. 2000. Role of the PI3K regulatory subunit in the control of actin organization and cell migration. J Cell Biol 151:249-262.
16. Kao AW, Noda Y, Johnson JH, Pessin JE, Saltiel AR. 1999. Aldolase mediates the association of F-actin with the insulin-responsive glucose transporter GLUT4. J Biol Chem 274:17742-17747.
17. Kim JH, Lee S, Lee TG, Hirata M, Suh PG, Ryu SH. 2002. Phospholipase D2 directly interacts with aldolase via its PH domain. Biochemistry 41:3414-3421.
18. Knight RJ, Kofoed KF, Schelbert HR, Buxton DB. 1996. Inhibition of glyceraldehyde-3-phosphate dehydrogenase in post-ischaemic myocardium.Cardiovasc Res 32:1016-1023.
19. Koppitz B, Vogel F, Mayr GW. 1986. Mammalian aldolases are isomerselective high-affinity inositol polyphosphate binders. Eur J Biochem 161:421-433.
20. Lu M, Ammar D, Ives H, Albrecht F, Gluck SL. 2007. Physical interaction between aldolase and vacuolar Ht -ATPase is essential for the assembly and activity of the proton pump. J Biol Chem 282:24495-24503.
21. Lu M, Holliday S, Zhang L, Dunn WA, Jr., Gluck SL. 2001. Interaction between aldolase and vacuolar Ht -ATPase: Evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 276:30407-30413.
22. Lu M, Sautin YY, Holliday LS, Gluck SL. 2004. The glycolytic enzyme aldolase mediates assembly, expression, and activity of vacuolar Ht -ATPase. J Biol Chem 279:8732-8739.
23. Lundmark R, Carlsson SR. 2003. Sorting nexin 9 participates in clathrinmediated endocytosis through interactions with the core components. J Biol Chem 278:46772-46781.
24. Lundmark R, Carlsson SR. 2004. Regulated membrane recruitment of dynamin-2 mediated by sorting nexin 9. J Biol Chem 279:42694-42702.
25. Martinez-Quiles N, Rohatgi R, Anton IM, Medina M, Saville SP, Miki H, Yamaguchi H, Takenawa T, Hartwig JH, Geha RS, Ramesh N. 2001. WIP regulates N-WASP-mediated actin polymerization and filopodium formation.Nat Cell Biol 3:484-491.
26. Merkulova M, Hurtado-Lorenzo A, Hosokawa H, Zhuang Z, Brown D, Ausiello DA, Marshansky V. 2011. Aldolase directly interacts with ARNO and modulates cell morphology and acidic vesicle distribution. Am J Physiol Cell Physiol 300:C1442-C1455.
27. Millard TH, Sharp SJ, Machesky LM. 2004. Signalling to actin assembly via the WASP (Wiskott.Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380:1-17.
28. Misra A, Lim RP, Wu Z, Thanabalu T. 2007. N-WASP plays a critical role in fibroblast adhesion and spreading. Biochem Biophys Res Commun 364:908-912.
29. Morris AJ. 1995. A proposed catalytic mechanism of rabbit aldolase a based upon site-directed mutagenesis. Boston University, Ph.D. Dissertation.
30. Morris AJ, Tolan DR. 1993. Site-directed mutagenesis identifies aspartate 33 as a previously unidentified critical residue in the catalytic mechanism of rabbit aldolase A. J Biol Chem 268:1095-1100.
31. Orosz F, Christova TY, Ovadi J. 1988a. Functional in vitro test of calmodulin antagonism: Effect of drugs on interaction between calmodulin and glycolytic enzymes. Mol Pharmacol 33:678-682.
32. Orosz F, Christova TY, Ovadi J. 1988b. Modulation of phosphofructokinase action by macromolecular interactions. Quantitative analysis of the phosphofructokinase-aldolase-calmodulin system. Biochim Biophys Acta 957:293-300.
33. Ottaway JH, Mowbray J. 1977. The role of compartmentation in the control of glycolysis. Curr Top Cell Regul 12:107-208.
34. Pagliaro L, Taylor DL. 1992. 2-Deoxyglucose and cytochalasin D modulate aldolase mobility in living 3T3 cells. J Cell Biol 118:859-863.
35. Pardee JD, Spudich JA. 1982. Purification of muscle actin. Methods Enzymol 85(PtB):164-181.
36. Penhoet EE, Kochman M, Valentine R, Rutter WJ. 1967. The subunit structure of mammalian fructose diphosphate aldolase. Biochemistry 6:2940-2949.
37. Ritterson Lew C. 2012. Non-glycolytic roles for aldolase in actin-dependent cellular processes. Boston University, Ph.D. Dissertation.
38. Ritterson Lew C, Tolan DR. 2012. Targeting of several glycolytic enzymes using RNA interference reveals aldolase affects cancer-cell proliferation through a non-glycolytic mechanism. J Biol Chem 287:42554-42563.
39. Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T, Takenawa T, Kirschner MW. 1999. The interaction between N-WASP and the Arp2/3 complex links Cdc42- dependent signals to actin assembly. Cell 97:221-231.
40. Schindler R, Weichselsdorfer E, Wagner O, Bereiter-Hahn J. 2001. Aldolaselocalization in cultured cells: Cell-type and substrate-specific regulation of cytoskeletal associations. Biochem Cell Biol 79:719-728.
41. Sibley LD. 2003. Toxoplasma gondii: Perfecting an intracellular life style. Traffic 4:581-586.
42. Singh P, Salih M, Leddy JJ, Tuana BS. 2004. The muscle-specific calmodulindependent protein kinase assembles with the glycolytic enzyme complex at the sarcoplasmic reticulum and modulates the activity of glyceraldehyde-3- phosphate dehydrogenase in a Ca2t/calmodulin-dependent manner. J Biol Chem 279:35176-35182.
43. St-Jean M, Izard T, Sygusch J. 2007. A hydrophobic pocket in the active site of glycolytic aldolase mediates interactions with Wiskott.Aldrich syndrome protein. J Biol Chem 282:14309-14315.
44. Sukow C, DeRosier DJ. 2003. Order, disorder, and perturbations in actinaldolase rafts. Biophys J 85:525-536.
45. Tochio T, Tanaka H, Nakata S, Hosoya H. 2010. Fructose-1,6-bisphosphate aldolase A is involved in HaCaT cell migration by inducing lamellipodia formation. J Dermatol Sci 58:123-129.
46. Tolan DR, Schuler B, Beernink PT, Jaenicke R. 2003. Thermodynamic analysis of the dissociation of the aldolase tetramer substituted at one or both of the subunit interfaces. Biol Chem 384:1463-1471.
47. Vetterkind S, Miki H, Takenawa T, Klawitz I, Scheidtmann KH, Preuss U. 2002. The rat homologue of Wiskott.Aldrich syndrome protein (WASP)-interacting protein (WIP) associates with actin filaments, recruits N-WASP from the nucleus, and mediates mobilization of actin from stress fibers in favor of filopodia formation. J Biol Chem 277:87-95.
48. Wang J, Morris AJ, Tolan DR, Pagliaro L. 1996. The molecular nature of the Factin binding activity of aldolase revealed with site-directed mutants. J Biol Chem 271:6861-6865.
49. Wang J, Tolan DR, Pagliaro L. 1997. Metabolic compartmentation in living cells: Structural association of aldolase. Exp Cell Res 237:445-451.
50. Wu X, Suetsugu S, Cooper LA, Takenawa T, Guan JL. 2004. Focal adhesion kinase regulation of N-WASP subcellular localization and function. J Biol Chem 279:9565-9576.