APIX is a trafficking regulator that balances recycling and degradation of the epidermal growth factor receptor

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Kortüm, Fanny ^a   Harms, Frederike Leonie ^a   Hennighausen, Natascha ^a   Rosenberger, Georg ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN ALPHAPIX; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ARHGEF6 PROTEIN, HUMAN; CBL PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR; PROTEIN BINDING; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BIOTINYLATION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ANIMAL; CHLOROCEBUS AETHIOPS; CHO CELL LINE; COS CELL LINE; CRICETULUS; HAMSTER; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; CRICETULUS; EPIDERMAL GROWTH FACTOR; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; UBIQUITINATION;

EID: 84941355774     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132737     Document Type: Article

References (87)

1. Kutsche K, Yntema H, Brandt A, Jantke I, Nothwang HG, Orth U, et al. Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nat Genet. 2000;26(2):247-50. Epub 2000/10/04. doi: 10.1038/80002 PMID: 11017088.
2. Bagrodia S, Taylor SJ, Jordon KA, Van Aelst L, Cerione RA. A novel regulatorof p21-activated kinases. J BiolChem. 1998;273(37):23633-6. PMID: 12496381.
3. Manser E, Loo TH, Koh CG, Zhao ZS, Chen XQ, Tan L, et al. PAK kinases are directly coupled to the PIXfamily of nucleotide exchange factors. Mol Cell. 1998;1(2):183-92. PMID: 9659915
4. Baird D, Feng Q, Cerione RA. The Cool-2/alpha-Pix protein mediates a Cdc42-Rac signaling cascade. CurrBiol. 2005;15(1):1-10. PMID: 15649357.
5. Feng Q, Baird D, Cerione RA. Novel regulatory mechanisms for the Dbl family guanine nucleotide exchange factor Cool-2/alpha-Pix. The EMBO journal. 2004;23(17):3492-504. Epub 2004/08/13. doi: 10.1038/sj.emboj.7600331 PMID: 15306850; PubMed Central PMCID: PMC516622.
6. Koh CG, Manser E, Zhao ZS, Ng CP, Lim L. Beta1PIX, the PAK-interacting exchange factor, requires localization via a coiled-coil region to promote microvillus-like structures and membrane ruffles. J Cell Sci. 2001;114(Pt23):4239-51. PMID: 11709153.
7. Feng Q, Albeck JG, Cerione RA, Yang W. Regulation of the Cool/Pix proteins: key binding partners of the Cdc42/Ractargets, the p21-activated kinases. J BiolChem. 2002;277(7):5644-50. Epub2001/12/14. doi: 10.1074/jbc. M107704200 PMID: 11741931.
8. Ramakers GJ, Wolfer D, Rosenberger G, Kuchenbecker K, Kreienkamp HJ, Prange-Kiel J, et al. Dysregulation of Rho GTPases in the alphaPix/Arhgef6 mouse model of X-linked intellectual disability is paralleled by impaired structural and synaptic plasticity and cognitive deficits. Human molecular genetics. 2012;21(2):268-86. Epub 2011/10/13. doi: 10.1093/hmg/ddr457 PMID: 21989057.
9. Rossman KL, der CJ, Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotideexchange factors. Nat Rev Mol Cell Biol. 2005;6(2):167-80. PMID: 15688002.
10. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420(6916):629-35. PMID: 12101119.
11. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9(9):690-701. PMID: 18719708. doi: 10.1038/nrm2476
12. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell DevBiol. 2005;21:247-69. PMID: 16212495.
13. Stofega MR, Sanders LC, Gardiner EM, Bokoch GM. Constitutive p21-activated kinase (PAK) activation in breast cancer cells as a result of mislocalization of PAK to focal adhesions. Mol Biol Cell. 2004;15(6):2965-77. PMID: 15047871.
14. Hua KT, Tan CT, Johansson G, Lee JM, Yang PW, Lu HY, et al. N-alpha-acetyltransferase 10 protein suppresses cancer cell metastasis by binding PIX proteins and inhibiting Cdc42/Rac1 activity. Cancer Cell. 2011;19(2):218-31. Epub 2011/02/08. doi: 10.1016/j.ccr.2010.11.010 PMID: 21295525.
15. Yoshimi R, Yamaji S, Suzuki A, Mishima W, Okamura M, Obana T, et al. The gamma-parvin-integrinlinked kinase complex is critically involved in leukocyte-substrate interaction. J Immunol. 2006;176(6):3611-24. Epub 2006/03/07. PMID: 16517730.
16. Rosenberger G, Gal A, Kutsche K. AlphaPIX associates with calpain 4, the small subunit of calpain, and has a dual role in integrin-mediated cell spreading. J Biol Chem. 2005;280(8):6879-89. Epub 2004/12/22. doi: 10.1074/jbc. M412119200 PMID: 15611136.
17. Rosenberger G, Jantke I, Gal A, Kutsche K. Interaction of alphaPIX (ARHGEF6) with beta-parvin (PARVB) suggests an involvement of alphaPIX in integrin-mediated signaling. Human molecular genetics. 2003;12(2):155-67. Epub 2002/12/25. PMID: 12499396.
18. Rosenberger G, Kutsche K. AlphaPIX and betaPIX and their role in focal adhesion formation. Eur J Cell Biol. 2006;85(3-4):265-74. Epub 2005/12/13. doi: 10.1016/j.ejcb.2005.10.007 PMID: 16337026.
19. Gringel A, Walz D, Rosenberger G, Minden A, Kutsche K, Kopp P, et al. PAK4 and alphaPIX determine podosome size and number in macrophages through localized actin regulation. Journal of cellular physiology. 2006;209(2):568-79. Epub 2006/08/10. doi: 10.1002/jcp. 20777 PMID: 16897755.
20. Korthals M, Schilling K, Reichardt P, Mamula D, Schluter T, Steiner M, et al. alphaPIX RhoGEFsupports positive selection by restraining migration and promoting arrest of thymocytes. J Immunol. 2014;192(7):3228-38. doi: 10.4049/jimmunol.1302585 PMID: 24591366.
21. Seong MW, Park JH, Yoo HM, Yang SW, Oh KH, Ka SH, et al. c-Cbl regulates alphaPix-mediated cell migration and invasion. Biochemical and biophysical research communications. 2014;455(3-4):153-8. doi: 10.1016/j.bbrc.2014.10.129 PMID: 25450678.
22. Li Z, Hannigan M, Mo Z, Liu B, Lu W, Wu Y, et al. Directional sensing requires G beta gamma-mediated PAK1 and PIX alpha-dependent activation of Cdc42. Cell. 2003;114(2):215-27. PMID: 12887923.
23. Mazaki Y, Hashimoto S, Tsujimura T, Morishige M, Hashimoto A, Aritake K, et al. Neutrophil direction sensing and superoxide production linked by the GTPase-activating protein GIT2. Nature immunology. 2006;7(7):724-31. Epub 2006/05/23. doi: 10.1038/ni1349 PMID: 16715100.
24. Totaro A, Tavano S, Filosa G, Gartner A, Pennucci R, Santambrogio P, et al. Biochemical and functional characterization of alphaPIX, a specific regulator of axonal and dendritic branching in hippocampal neurons. Biol Cell. 2012. Epub 2012/05/03. doi: 10.1111/boc.201200006 PMID: 22548323.
25. Node-Langlois R, Muller D, Boda B. Sequential implication of the mental retardation proteins ARH-GEF6 and PAK3 in spine morphogenesis. J Cell Sci. 2006;119(Pt 23):4986-93. Epub 2006/11/16. doi: 10.1242/jcs.03273 PMID: 17105769.
26. Phee H, Abraham RT, Weiss A. Dynamic recruitment of PAK1 to the immunological synapse is mediated by PIX independently of SLP-76 and Vav1. Nature immunology. 2005;6(6):608-17. PMID: 15864311.
27. Missy K, Hu B, Schilling K, Harenberg A, Sakk V, Kuchenbecker K, et al. AlphaPIX Rho GTPase guanine nucleotide exchange factor regulates lymphocyte functions and antigen receptor signaling. Mol Cell Biol. 2008;28(11):3776-89. Epub 2008/04/02. doi: 10.1128/MCB.00507-07 PMID: 18378701; PubMed Central PMCID: PMC2423308.
28. Yoshii S, Tanaka M, Otsuki Y, Wang DY, Guo RJ, Zhu Y, et al. alphaPIX nucleotide exchange factor is activated by interaction with phosphatidylinositol 3-kinase. Oncogene. 1999;18(41):5680-90. Epub 1999/10/19. doi: 10.1038/sj.onc.1202936 PMID: 10523848.
29. Kong KF, Fu G, Zhang Y, Yokosuka T, Casas J, Canonigo-Balancio AJ, et al. Protein kinaseC-etacontrols CTLA-4-mediated regulatory T cell function. Nature immunology. 2014;15(5):465-72. doi: 10. 1038/ni.2866 PMID: 24705298; PubMed Central PMCID: PMC4040250.
30. Llavero F, Urzelai B, Osinalde N, Galvez P, Lacerda HM, Parada LA, et al. Guanine nucleotide exchange factor alphaPIX leads to activation of the Rac 1 GTPase/Glycogen phosphorylase pathway in Interleukin (IL)-2-stimulatedTcells. J Biol Chem. 2015. doi: 10.1074/jbc. M114.608414 PMID: 25694429.
31. Flanders JA, Feng Q, Bagrodia S, Laux MT, Singavarapu A, Cerione RA. The Cbl proteins are binding partners for the Cool/Pix family of p21-activated kinase-binding proteins. FEBS Lett. 2003;550(1-3):119-23. Epub 2003/08/26. PMID: 12935897.
32. Schmidt MH, Dikic I. The Cbl interactome and its functions. Nat Rev Mol Cell Biol. 2005;6(12):907-19. PMID: 16227975.
33. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol. 2001;2(4):294-307. PMID: 11283727.
34. Thien CB, Langdon WY. Negative regulation of PTK signalling by Cbl proteins. Growth factors (Chur, Switzerland). 2005;23(2):161-7. PMID: 16019438.
35. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol. 2001;2(3):169-78. PMID: 11265246.
36. Staub O, Rotin D. Role of ubiquitylation in cellular membrane transport. Physiological reviews. 2006;86(2):669-707. PMID: 16601271.
37. Dikic I, Szymkiewicz I, Soubeyran P. Cbl signaling networks in the regulation of cell function. Cell Mol Life Sci. 2003;60(9):1805-27. PMID: 14523545.
38. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res. 2009;315(4):683-96. PMID: 19278030.
39. Swaminathan G, Tsygankov AY. The Cbl family proteins: ring leaders in regulation of cell signaling. J Cell Physiol. 2006;209(1):21-43. PMID: 16741904.
40. Wu WJ, Tu S, Cerione RA. Activated Cdc42 sequesters c-Cbl and prevents EGF receptor degradation. Cell. 2003;114(6):715-25. PMID: 14505571.
41. Feng Q, Baird D, Peng X, Wang J, Ly T, Guan JL, et al. Cool-1 functions as an essential regulatory node for EGF receptor- and Src-mediated cell growth. Nat Cell Biol. 2006;8(9):945-56. PMID: 16892055.
42. Schmidt MH, Husnjak K, Szymkiewicz I, Haglund K, Dikic I. Cbl escapes Cdc42-mediated inhibition by downregulationofthe adaptor molecule betaPix. Oncogene. 2006;25(21):3071-8. PMID: 16407834.
43. Bagrodia S, Bailey D, Lenard Z, Hart M, Guan JL, Premont RT, et al. Atyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J Biol Chem. 1999;274(32):22393-400. PMID: 10428811.
44. Turner CE, Brown MC, Perrotta JA, Riedy MC, Nikolopoulos SN, McDonald AR, et al. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: A role in cytoskeletal remodeling. J Cell Biol. 1999;145(4):851-63. PMID: 10330411.
45. Schlenker O, Rittinger K. Structures of dimericGIT1 and trimeric beta-PIX and implications for GIT-PIX complex assembly. J Mol Biol. 2009;386(2):280-9. doi: 10.1016/j.jmb.2008.12.050 PMID: 19136011.
46. Waterman H, Levkowitz G, Alroy I, Yarden Y. The RING finger of c-Cbl mediates desensitizationofthe epidermal growth factor receptor. J Biol Chem. 1999;274(32):22151-4. PMID: 10428778.
47. Lin Q, Yang W, Cerione RA. Measurement of epidermal growth factor receptor turnover and effects of Cdc42. Methods Enzymol. 2006;406:614-25. Epub 2006/02/14. doi: 10.1016/S0076-6879 (06) 06048-4 PMID: 16472692.
48. Sorkin A, Duex JE. Quantitative analysis of endocytosis and turnover of epidermal growth factor (EGF) and EGF receptor. Current protocols in cell biology/editorial board, Juan S Bonifacino [etal]. 2010; Chapter 15:Unit 15 4. PMID: 20235100.
49. Schmidt MH, Dikic I. Assays to monitor degradation of the EGF receptor. Methods Mol Biol. 2006;327:131-8. PMID: 16780217.
50. Roepstorff K, Grandal MV, Henriksen L, Knudsen SL, Lerdrup M, Grovdal L, et al. Differential effects of EGFRligandson endocytic sorting of the receptor. Traffic. 2009;10(8):1115-27. Epub 2009/06/18. doi: 10.1111/j.1600-0854.2009.00943.x PMID: 19531065; PubMed Central PMCID: PMC2723868.
51. Shtiegman K, Kochupurakkal BS, Zwang Y, Pines G, Starr A, Vexler A, et al. Defective ubiquitinylation of EGFR mutants of lung cancer confers prolonged signaling. Oncogene. 2007;26(49):6968-78. Epub 2007/05/09. doi: 10.1038/sj.onc.1210503 PMID: 17486068.
52. Turvy DN, Blum JS. Biotin labeling and quantitation of cell-surface proteins. Curr Protoc Immunol. 2001; Chapter 18:Unit 18 7. Epub 2008/04/25. doi: 10.1002/0471142735.im1807s36 PMID: 18432749.
53. Van Weert AW, Geuze HJ, Groothuis B, Stoorvogel W. Primaquine interferes with membrane recycling from endosomes to the plasma membrane through a direct interaction with endosomes which does not involve neutralisation of endosomal pH nor osmotic swelling of endosomes. Eur J Cell Biol. 2000;79(6):394-9. Epub 2000/08/06. PMID: 10928454.
54. Wiley HS, Burke PM. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic. 2001;2(1):12-8. Epub 2001/02/24. PMID: 11208164.
55. Wong RW, Guillaud L. The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev. 2004;15(2-3):147-56. Epub 2004/04/28. doi: 10.1016/j.cytogfr.2004.01.004 PMID: 15110798.
56. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol. 2001;2(2):127-37. doi: 10.1038/35052073 PMID: 11252954.
57. Sigismund S, Confalonieri S, Ciliberto A, Polo S, Scita G, Di Fiore PP. Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiological reviews. 2012;92(1):273-366. Epub 2012/02/03. doi: 10.1152/physrev. 00005.2011 PMID: 22298658.
58. Platta HW, Stenmark H. Endocytosis and signaling. Curr Opin Cell Biol. 2011;23(4):393-403. Epub 2011/04/09. doi: 10.1016/j.ceb.2011.03.008 PMID: 21474295.
59. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol. 2009;10(9):597-608. Epub 2009/08/22. doi: 10.1038/nrm2755 PMID: 19696797; PubMed Central PMCID: PMC3038567.
60. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol. 2004;5(2):121-32. Epub 2004/03/26. doi: 10.1038/nrm1315 PMID: 15040445.
61. Sorkin A, Von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol. 2009;10(9):609-22. Epub 2009/08/22. doi: 10.1038/nrm2748 PMID: 19696798; PubMed Central PMCID: PMC2895425.
62. Scita G, Di Fiore PP. The endocytic matrix. Nature. 2010;463(7280):464-73. Epub 2010/01/30. doi: 10.1038/nature08910 PMID: 20110990.
63. Dikic I. Mechanisms controlling EGF receptor endocytosis and degradation. Biochem Soc Trans. 2003;31(Pt6):1178-81. Epub 2003/12/04. PMID: 14641021.
64. Eden ER, Huang F, Sorkin A, Futter CE. The role of EGF receptor ubiquitination in regulating its intracellular traffic. Traffic. 2012;13(2):329-37. doi: 10.1111/j.1600-0854.2011.01305.x PMID: 22017370; PubMed Central PMCID: PMC3261333.
65. Gruenberg J, Stenmark H. The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol. 2004;5(4):317-23. doi: 10.1038/nrm1360 PMID: 15071556.
66. Qualmann B, Mellor H. Regulation of endocytic traffic by RhoGTPases. Biochem J. 2003;371(Pt 2):233-41. PMID: 12564953.
67. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 2006;16(10):522-9. Epub 2006/09/05. doi: 10.1016/j.tcb.2006.08.006 PMID: 16949823.
68. Zhao ZS, Manser E, Loo TH, Lim L. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol. 2000;20(17):6354-63. PMID: 10938112.
69. Hoefen RJ, Berk BC. The multifunctional GIT family of proteins. J Cell Sci. 2006;119(Pt 8):1469-75. Epub 2006/04/07. doi: 10.1242/jcs.02925 PMID: 16598076.
70. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol. 2006;7(5):347-58. Epub 2006/04/25. doi: 10.1038/nrm1910 PMID: 16633337.
71. Vitale N, Patton WA, Moss J, Vaughan M, Lefkowitz RJ, Premont RT. GIT proteins, A novel family of phosphatidylinositol 3, 4, 5-trisphosphate-stimulated GTPase-activating proteins for ARF6. J Biol Chem. 2000;275(18):13901-6. Epub 2000/05/02. PMID: 10788515.
72. Premont RT, Claing A, Vitale N, Perry SJ, Lefkowitz RJ. The GIT family of ADP-ribosylation factor GTPase-activating proteins. Functional diversity of GIT2 through alternative splicing. J Biol Chem. 2000;275(29):22373-80. Epub 2000/07/18. PMID: 10896954.
73. Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol. 2011;12(6):362-75. Epub 2011/05/19. doi: 10.1038/nrm3117 PMID: 21587297; PubMed Central PMCID: PMC3245550.
74. Frank SR, Hansen SH. The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin Cell Biol. 2008;19(3):234-44. Epub 2008/02/27. doi: 10.1016/j.semcdb.2008.01.002 PMID: 18299239; PubMed Central PMCID: PMC2394276.
75. Di Cesare A, Paris S, Albertinazzi C, Dariozzi S, Andersen J, Mann M, et al. p95-APP1 links membrane transport to Rac-mediated reorganization of actin. Nat Cell Biol. 2000;2(8):521-30. PMID: 10934473.
76. Matafora V, Paris S, Dariozzi S, De Curtis I. Molecular mechanisms regulating the subcellular localization of p95-APP1 between the endosomal recycling compartment and sites of actin organization at the cell surface. J Cell Sci. 2001;114(Pt24):4509-20. PMID: 11792816.
77. Valdes JL, Tang J, McDermott MI, Kuo JC, Zimmerman SP, Wincovitch SM, et al. Sorting nexin 27 protein regulates trafficking of a p21-activated kinase (PAK) interacting exchange factor (beta-Pix)-G protein-coupled receptor kinase interacting protein (GIT) complex via a PDZ domain interaction. J Biol Chem. 2011;286(45):39403-16. Epub 2011/09/20. doi: 10.1074/jbc. M111.260802 PMID: 21926430; PubMed Central PMCID: PMC3234764.
78. Prelich G. Gene overexpression: uses, mechanisms, and interpretation. Genetics. 2012;190(3):841-54. doi: 10.1534/genetics.111.136911 PMID: 22419077; PubMed Central PMCID: PMC3296252.
79. Sorkin A. Endocytosis and intracellular sorting of receptor tyrosine kinases. Front Biosci. 1998;3:d729-38. Epub 1998/07/22. PMID: 9671598.
80. Bitler BG, Goverdhan A, Schroeder JA. MUC1 regulates nuclear localization and function of the epidermal growth factor receptor. J Cell Sci. 2010;123(Pt 10):1716-23. Epub 2010/04/22. doi: 10.1242/jcs. 062661 PMID: 20406885; PubMed Central PMCID: PMC2864713.
81. Yarden Y. The EGFR family and its ligands in human cancer.signalling mechanisms and therapeutic opportunities. Eur J Cancer. 2001;37 Suppl 4:S3-8. Epub 2001/10/13. PMID: 11597398.
82. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature. 2001;411(6835):355-65. Epub 2001/05/18. doi: 10.1038/35077225 PMID: 11357143.
83. Roepstorff K, Grovdal L, Grandal M, Lerdrup M, Van Deurs B. Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem Cell Biol. 2008;129(5):563-78. Epub 2008/02/22. doi: 10.1007/s00418-008-0401-3 PMID: 18288481; PubMed Central PMCID: PMC2323030.
84. Grovdal LM, Johannessen LE, Rodland MS, Madshus IH, Stang E. Dysregulation of Ack1 inhibits down-regulation of the EGF receptor. Exp Cell Res. 2008;314(6):1292-300. Epub 2008/02/12. doi: 10. 1016/j.yexcr.2007.12.017 PMID: 18262180.
85. Yokota T, Kouno J, Adachi K, Takahashi H, Teramoto A, Matsumoto K, et al. Identification of histological markers for malignant glioma by genome-wide expression analysis: dynein, alpha-PIX and sorcin. Acta Neuropathol. 2006;111(1):29-38. Epub 2005/12/02. doi: 10.1007/s00401-005-1085-6 PMID: 16320026.
86. Daniels RH, Zenke FT, Bokoch GM. alphaPix stimulates p21-activated kinase activity through exchange factor-dependent and-independent mechanisms. J Biol Chem. 1999;274(10):6047-50. Epub 1999/02/26. PMID: 10037684.
87. Yoshii S, Tanaka M, Otsuki Y, Fujiyama T, Kataoka H, Arai H, et al. Involvement of alpha-PAK-interacting exchange factor in the PAK1-c-Jun. NH (2)-terminal kinase 1 activation and apoptosis induced by benzo[a]pyrene. Mol Cell Biol. 2001;21(20):6796-807. Epub 2001/09/21. doi: 10.1128/MCB.21.20. 6796-6807.2001 PMID: 11564864; PubMed Central PMCID: PMC99857.