Arf1 and Arf6 promote ventral actin structures formed by acute activation of protein kinase C and Src

Cytoskeleton

Volumn 71, Issue 6, 2014, Pages 380-394

  Caviston, Juliane P ^a   Cohen, Lee Ann ^a   Donaldson, Julie G ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Arf1; Cortical actin; PKC; Src; Ventral surface

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTOR 6; PROTEIN KINASE C; PROTEIN TYROSINE KINASE;

BRONCHUS; CELL LINE; CYTOLOGY; CYTOSKELETON; ENZYME ACTIVATION; HELA CELL LINE; HUMAN; METABOLISM;

ACTINS; ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; BRONCHI; CELL LINE; CYTOSKELETON; ENZYME ACTIVATION; HELA CELLS; HUMANS; PROTEIN KINASE C; SRC-FAMILY KINASES;

EID: 84904408455     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21181     Document Type: Article

References (74)

1. Aikawa Y, Martin TFJ. 2003. ARF6 regulates a plasma membrane pool of phosphatidylinositol(4, 5)bisphosphate required for regulated exocytosis. J Cell Biol 162(4):647-659.
2. Albiges-Rizo C, Destaing O, Fourcade B, Planus E, Block MR. 2009. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J Cell Sci 122(Pt 17):3037-3049.
3. Balasubramanian N, Scott DW, Castle JD, Casanova JE, Schwartz MA. 2007. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat Cell Biol 9(12):1381-1391.
4. Beemiller P, Hoppe AD, Swanson JA. 2006. A phosphatidylinositol-3-kinase-dependent signal transition regulates ARF1 and ARF6 during Fcgamma receptor-mediated phagocytosis. PLoS Biol 4(6):e162.
5. Bharti S, Inoue H, Bharti K, Hirsch DS, Nie Z, Yoon HY, Artym V, Yamada KM, Mueller SC, Barr VA, et al. 2007. Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol Cell Biol 27(23):8271-8283.
6. Block MR, Badowski C, Millon-Fremillon A, Bouvard D, Bouin AP, Faurobert E, Gerber-Scokaert D, Planus E, Albiges-Rizo C. 2008. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur J Cell Biol 87(8-9):491-506.
7. Boshans RL, Szanto S, van Aelst L, D'Souza-Schorey C. 2000. ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol Cell Biol 20(10):3685-3694.
8. Boulay PL, Cotton M, Melancon P, Claing A. 2008. ADP-ribosylation factor 1 controls the activation of the phosphatidylinositol 3-kinase pathway to regulate epidermal growth factor-dependent growth and migration of breast cancer cells. J Biol Chem 283(52):36425-36434.
9. Brandt DT, Goerke A, Heuer M, Gimona M, Leitges M, Kremmer E, Lammers R, Haller H, Mischak H. 2003. Protein kinase C delta induces Src kinase activity via activation of the protein tyrosine phosphatase PTP alpha. J Biol Chem 278(36):34073-34078.
10. Bretschneider T, Diez S, Anderson K, Heuser J, Clarke M, Muller-Taubenberger A, Kohler J, Gerisch G. 2004. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol 14(1):1-10.
11. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. 2001. Phosphatidylinositol 4, 5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 154(5):1007-1017.
12. Brown HA, Gutowski S, Moomaw CR, Slaughter C, Sternweis PC. 1993. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75(6):1137-1144.
13. Brown MT, Andrade J, Radhakrishna H, Donaldson JG, Cooper JA, Randazzo PA. 1998. ASAP1, a phospholipid-dependent arf GTPase-activating protein that associates with and is phosphorylated by Src. Mol Cell Biol 18(12):7038-7051.
14. Caldieri G, Buccione R. 2010. Aiming for invadopodia: organizing polarized delivery at sites of invasion. Trends Cell Biol 20(2):64-70.
15. Cao H, Weller S, Orth JD, Chen J, Huang B, Chen JL, Stamnes M, McNiven MA. 2005. Actin and Arf1-dependent recruitment of a cortactin-dynamin complex to the Golgi regulates post-Golgi transport. Nat Cell Biol 7(5):483-492.
16. Casanova JE. 2007. Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8(11):1476-1485.
17. Case LB, Waterman CM. 2011. Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PLoS One 6(11):e26631.
18. Cockcroft S, Thomas GM, Fensome A, Geny B, Cunningham E, Gout I, Hiles I, Totty NF, Truong O, Hsuan JJ. 1994. Phospholipase D: a downstream effector of ARF in granulocytes. Science 263(5146):523-526.
19. Cohen LA, Honda A, Varnai P, Brown FD, Balla T, Donaldson JG. 2007. Active Arf6 recruits ARNO/cytohesin GEFs to the PM by binding their PH domains. Mol Biol Cell 18(6):2244-2253.
20. D'Souza-Schorey C, Chavrier P. 2006. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7(5):347-358.
21. Daher Z, Boulay PL, Desjardins F, Gratton JP, Claing A. 2010. Vascular endothelial growth factor receptor-2 activates ADP-ribosylation factor 1 to promote endothelial nitric-oxide synthase activation and nitric oxide release from endothelial cells. J Biol Chem 285(32):24591-24599.
22. Dascher C, Balch WE. 1994. Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J Biol Chem 269(2):1437-1448.
23. Donaldson JG, Honda A, Weigert R. 2005. Multiple activities for Arf1 at the Golgi complex. Biochim Biophys Acta 1744(3):364-373.
24. Donaldson JG, Jackson CL. 2011. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nature Rev Mol Cell Biol 12(6):362-375.
25. Donaldson JG, Porat-Shliom N, Cohen LA. 2009. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21(1):1-6.
26. Dubois T, Paleotti O, Mironov AA, Fraisier V, Stradal TE, De Matteis MA, Franco M, Chavrier P. 2005. Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat Cell Biol 7(4):353-364.
27. Eyster CA, Higginson JD, Huebner R, Porat-Shliom N, Weigert R, Wu WW, Shen RF, Donaldson JG. 2009. Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 10(5):590-599.
28. Franco M, Peters PJ, Boretto J, van Donselaar E, Neri A, D'Souza-Schorey C, Chavrier P. 1999. EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. Embo J 18(6):1480-1491.
29. Frank SR, Hatfield JC, Casanova JE. 1998. Remodeling of the actin cytoskeleton is coordinately regulated by protein kinase C and the ADP-ribosylation factor nucleotide exchange factor ARNO. Mol Biol Cell 9(11):3133-3146.
30. Fucini RV, Navarrete A, Vadakkan C, Lacomis L, Erdjument-Bromage H, Tempst P, Stamnes M. 2000. Activated ADP-ribosylation factor assembles distinct pools of actin on golgi membranes. J Biol Chem 275(25):18824-18829.
31. Gavazzi I, Nermut MV, Marchisio PC. 1989. Ultrastructure and gold-immunolabelling of cell-substratum adhesions (podosomes) in RSV-transformed BHK cells. J Cell Sci 94 (Pt 1):85-99.
32. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA. 1999. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4, 5)P2 on the Golgi complex. Nat Cell Biol 1(5):280-287.
33. Grant BD, Donaldson JG. 2009. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10(9):597-608.
34. Hasegawa J, Tsujita K, Takenawa T, Itoh T. 2012. ARAP1 regulates the ring size of circular dorsal ruffles through Arf1 and Arf5. Mol Biol Cell 23(13):2481-2489.
35. Hashimoto S, Onodera Y, Hashimoto A, Tanaka M, Hamaguchi M, Yamada A, Sabe H. 2004. Requirement for Arf6 in breast cancer invasive activities. Proc Natl Acad Sci USA 101(17):6647-6652.
36. Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9(9):690-701.
37. Hernandez-Deviez DJ, Casanova JE, Wilson JM. 2002. Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci 5(7):623-624.
38. Hernandez-Deviez DJ, Roth MG, Casanova JE, Wilson JM. 2004. ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase {alpha}. Mol Biol Cell 15(1):111-120.
39. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, et al. 1999. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99(5):521-532.
40. Hu B, Shi B, Jarzynka MJ, Yiin JJ, D'Souza-Schorey C, Cheng SY. 2009. ADP-ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway. Cancer Res 69(3):794-801.
41. Humphreys D, Liu T, Davidson AC, Hume PJ, Koronakis V. 2012. The Drosophila Arf1 homologue Arf79F is essential for lamellipodium formation. J Cell Sci 125(Pt 23):5630-5635.
42. Jackson TR, Brown FD, Nie Z, Miura K, Foroni L, Sun J, Hsu VW, Donaldson JG, Randazzo PA. 2000. ACAPs are arf6 GTPase-activating proteins that function in the cell periphery. J Cell Biol 151(3):627-638.
43. Jovanovic OA, Brown FD, Donaldson JG. 2006. An effector domain mutant of Arf6 implicates phospholipase D in endosomal membrane recycling. Mol Biol Cell 17(1):327-335.
44. Klarlund JK, Tsiaras W, Holik JJ, Chawla A, Czech MP. 2000. Distinct polyphosphoinositide binding selectivities for pleckstrin homology domains of GRP1-like proteins based on diglycine versus triglycine motifs. J Biol Chem 275(42):32816-32821.
45. Koo TH, Eipper BA, Donaldson JG. 2007. Arf6 recruits the Rac GEF Kalirin to the plasma membrane facilitating Rac activation. BMC Cell Biol 8:29.
46. Koronakis V, Hume PJ, Humphreys D, Liu T, Horning O, Jensen ON, McGhie EJ. 2011. WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc Natl Acad Sci USA 108(35):14449-14454.
47. Ktistakis NT, Brown HA, Sternweis PC, Roth MG. 1995. Phospholipase D is present on Golgi-enriched membranes and its activation by ADP ribosylation factor is sensitive to brefeldin A. Proc Natl Acad Sci USA 92(11):4952-4956.
48. Kumari S, Mayor S. 2008. ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 10(1):30-41.
49. Lewis-Saravalli S, Campbell S, Claing A. 2013. ARF1 controls Rac1 signaling to regulate migration of MDA-MB-231 invasive breast cancer cells. Cell Signal 25(9):1813-1839.
50. Liu Y, Loijens JC, Martin KH, Karginov AV, Parsons JT. 2002. The association of ASAP1, an ADP ribosylation factor-GTPase activating protein, with focal adhesion kinase contributes to the process of focal adhesion assembly. Mol Biol Cell 13(6):2147-2156.
51. Macia E, Chabre M, Franco M. 2001. Specificities for the small G proteins ARF1 and ARF6 of the guanine nucleotide exchange factors ARNO and EFA6. J Biol Chem 276(27):24925-24930.
52. Macia E, Partisani M, Favard C, Mortier E, Zimmermann P, Carlier MF, Gounon P, Luton F, Franco M. 2008. The pleckstrin homology domain of the Arf6-specific exchange factor EFA6 localizes to the plasma membrane by interacting with phosphatidylinositol 4, 5-bisphosphate and F-actin. J Biol Chem 283(28):19836-19844.
53. Palacios F, Price L, Schweitzer J, Collard JG, D'Souza-Schorey C. 2001. An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. Embo J 20(17):4973-4986.
54. Porat-Shliom N, Kloog Y, Donaldson JG. 2008. A unique platform for H-Ras signaling involving clathrin-independent endocytosis. Mol Biol Cell 19(3):765-775.
55. Powelka AM, Sun J, Li J, Gao M, Shaw LM, Sonnenberg A, Hsu VW. 2004. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 5(1):20-36.
56. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat Methods 5(7):605-607.
57. Rocca DL, Amici M, Antoniou A, Suarez EB, Halemani N, Murk K, McGarvey J, Jaafari N, Mellor JR, Collingridge GL, et al. 2013. The small GTPase Arf1 modulates Arp2/3-mediated actin polymerization via PICK1 to regulate synaptic plasticity. Neuron 79(2):293-307.
58. Rozelle AL, Machesky LM, Yamamoto M, Driessens MH, Insall RH, Roth MG, Luby-Phelps K, Marriott G, Hall A, Yin HL. 2000. Phosphatidylinositol 4, 5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr Biol 10(6):311-320.
59. Sabe H, Hashimoto S, Morishige M, Ogawa E, Hashimoto A, Nam JM, Miura K, Yano H, Onodera Y. 2009. The EGFR-GEP100-Arf6-AMAP1 signaling pathway specific to breast cancer invasion and metastasis. Traffic 10(8):982-993.
60. Santy LC, Casanova JE. 2001. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J Cell Biol 154(3):599-610.
61. Santy LC, Frank SR, Casanova JE. 2001. Expression and analysis of ARNO and ARNO mutants and their effects on ADP-ribosylation factor (ARF)-mediated actin cytoskeletal rearrangements. Methods Enzymol 329:256-264.
62. Santy LC, Ravichandran KS, Casanova JE. 2005. The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation to the downstream activation of Rac1. Curr Biol 15(19):1749-1754.
63. Schafer DA, D'Souza-Schorey C, Cooper JA. 2000. Actin assembly at membranes controlled by ARF6. Traffic 1(11):892-903.
64. Song J, Khachikian Z, Radhakrishna H, Donaldson JG. 1998. Localization of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J Cell Sci 111(Pt 15):2257-2267.
65. Svensson HG, West MA, Mollahan P, Prescott AR, Zaru R, Watts C. 2008. A role for ARF6 in dendritic cell podosome formation and migration. Eur J Immunol 38(3):818-828.
66. Tague SE, Muralidharan V, D'Souza-Schorey C. 2004. ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc Natl Acad Sci USA 101(26):9671-9676.
67. Tatin F, Varon C, Genot E, Moreau V. 2006. A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci 119(Pt 4):769-781.
68. Teal SB, Hsu VW, Peters PJ, Klausner RD, Donaldson JG. 1994. An activating mutation in ARF1 stabilizes coatomer binding to Golgi membranes. J Biol Chem 269(5):3135-3138.
69. Volpicelli-Daley LA, Li Y, Zhang CJ, Kahn RA. 2005. Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol Biol Cell 16(10):4495-4508.
70. Whatmore J, Morgan CP, Cunningham E, Collison KS, Willison KR, Cockcroft S. 1996. ADP-ribosylation factor 1-regulated phospholipase D activity is localized at the plasma membrane and intracellular organelles in HL60 cells. Biochem J 320 (Pt 3):785-794.
71. Wu M, Wu X, De Camilli P. 2013. Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations. Proc Natl Acad Sci USA 110(4):1339-1344.
72. Xiao H, Bai XH, Kapus A, Lu WY, Mak AS, Liu M. 2010. PKC cascade regulates recruitment of MMP-9 to podosomes and its release and activation. Mol Cell Biol 30(23):5545-5561.
73. Xiao H, Eves R, Yeh C, Kan W, Xu F, Mak AS, Liu M. 2009. Phorbol ester-induced podosomes in normal human bronchial epithelial cells. J Cell Physiol 218(2):366-375.
74. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, Coomans C, Schulz J, N'Kuli F, Courtoy PJ, David G. 2005. Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf6. Dev Cell 9(3):377-388.