An unrecognized extracellular function for an intracellular adapter protein released from the cytoplasm into the tumor microenvironment

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 7, 2009, Pages 2182-2187

  Mintz, Paul J ^a,d   Cardó Vila, Marina ^a   Ozawa, Michael G ^a   Hajitou, Amin ^a,d   Rangel, Roberto ^a   Guzman Rojas, Liliana ^a   Christianson, Dawn R ^a   Arap, Marco A ^a,e   Giordano, Ricardo J ^a   Souza, Glauco R ^a   Easley, Jeffrey ^a,f   Salameh, Ahmad ^a,b   Oliviero, Salvatore ^b   Brentani, Ricardo R ^c   Koivunen, Erkki ^a   Arap, Wadih ^a   Pasqualini, Renata ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF SIENA   (Italy)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cancer; CrkL; Integrin; Phage display

Indexed keywords

BETA1 INTEGRIN; CRK LIKE PROTEIN; PEPTIDE LIBRARY; PLEXIN; PROTEIN SH2; PROTEIN SH3; SEMAPHORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL GROWTH; CELL SURFACE; CELL SURVIVAL; COMBINATORIAL LIBRARY; CONTROLLED STUDY; CYTOPLASM; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; LIGAND BINDING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR PROMOTION; TUMOR XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL LINE, TUMOR; CYTOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; NEOPLASMS; NUCLEAR PROTEINS; SRC HOMOLOGY DOMAINS;

MAMMALIA; MUS;

EID: 60549089200     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0807543105     Document Type: Article

References (48)

1. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37-44.
2. Cho W, Stahelin RV (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 34:119-151.
3. Martin KH, Slack JK, Boerner SA, Martin CC, Parsons JT (2002) Integrin connections map: To infinity and beyond. Science 296:1652-1653.
4. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912-1934.
5. Mochly-Rosen D (1995) Localization of protein kinases by anchoring proteins: A theme in signal transduction. Science 268:247-251.
6. Miller-Jensen K, Janes KA, Brugge JS, Lauffenburger DA (2007) Common effector processing mediates cell-specific responses to stimuli. Nature 448:604-608.
7. Hunter T (2007) The age of cross-talk: Phosphorylation, ubiquitination, and beyond. Mol Cell 28:730-738.
8. Pawson T, Scott JD (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
9. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signaling. Nature 411:355-365.
10. Hajitou A, et al. (2006) A hybrid vector for ligand-directed tumor targeting and molecular imaging. Cell 125:385-398.
11. Arap W, et al. (2002) Steps toward mapping the human vasculature by phage display. Nat Med 8:121-127.
12. Arap W, Pasqualini R, Ruoslahti E (1998) Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279:377-380.
13. Arap MA, et al. (2004) Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 6:275-284.
14. Pasqualini R, Ruoslahti E (1996) Organ targeting in vivo using phage display peptide libraries. Nature 380:364-366.
15. Pasqualini R, Arap W, Rajotte D, Ruoslahti E (2001) in Phage Display: A Laboratory Manual, eds Barbas CF, III, Burton DR, Scott JK, Silverman GJ (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), pp 22.1-22.24.
16. Giordano RJ, Cardó-Vila M, Lahdenranta J, Pasqualini R, Arap W (2001) Biopanning and rapid analysis of selective interactive ligands. Nat Med 7:1249-1253.
17. Ellerby HM, et al. (1999) Anticancer activity of targeted proapoptotic peptides. Nat Med 5:1032-1038.
18. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10:625-632.
19. Zurita AJ, et al. (2004) Combinatorial screenings in patients: The interleukin-11 receptor α as a candidate target in the progression of human prostate cancer. Cancer Res 64:435-439.
20. Shi M, et al. (2005) The crystal structure of the plexin-semaphorin-integrin domain/ hybrid domain/I-EGF1 segment from the human integrin β2 subunit at 1.8-Å resolution. J Biol Chem 280:30586-30593.
21. Mould AP, et al. (2005) Evidence that monoclonal antibodies directed against the integrin β subunit plexin/semaphorin/integrin domain stimulate function by inducing receptor extension. J Biol Chem 280:4238-4246.
22. Arnaout MA, Mahalingam B, Xiong JP (2005) Integrin structure, allostery, and bidirectional signaling. Annu Rev Cell Dev Biol 21:381-410.
23. ten Hoeve J, Morris C, Heisterkamp N, Groffen J (1993) Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene 8:2469-2474.
24. Harkiolaki M, Gilbert RJ, Jones EY, Feller SM (2006) The C-terminal SH3 domain of CRKL as a dynamic dimerization module transiently exposing a nuclear export signal. Structure (London)14:1741-1753.
25. Mayer BJ (2001) SH3 domains: Complexity in moderation. J Cell Sci 114:1253-1263.
26. Sicheri F, Moarefi I, Kuriyan J (1997) Crystal structure of the Src family tyrosine kinase Hck. Nature 385:602-609.
27. Kato M, Miyazawa K, Kitamura N (2000) A deubiquitinating enzyme UBPY interacts with the Src homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP. J Biol Chem 275:37481-37487.
28. Xu W, Harrison SC, Eck MJ (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385:595-602.
29. Liu Q, et al. (2003) Structural basis for specific binding of the Gads SH3 domain to an RxxK motif-containing SLP-76 peptide: A novel mode of peptide recognition. Mol Cell 11:471-481.
30. Walter P, Gilmore R, Blobel G (1984) Protein translocation across the endoplasmic reticulum. Cell 38:5-8.
31. Prudovsky I, et al. (2003) The nonclassical export routes: FGF1 and IL-1α point the way. J Cell Sci 116:4871-4881.
32. Reynwar BJ, et al. (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:461-464.
33. McNiven MA, Thompson HM (2006) Vesicle formation at the plasma membrane and trans-Golgi network: The same but different. Science 313:1591-1594.
34. Flieger O, et al. (2003) Regulated secretion of macrophage migration inhibitory factor is mediated by a nonclassical pathway involving an ABC transporter. FEBS Lett 551:78-86.
35. Hamon Y, et al. (1997) Interleukin-1β secretion is impaired by inhibitors of the ATP binding cassette transporter, ABC1. Blood 90:2911-2915.
36. Kishan KV, Scita G, Wong WT, Di Fiore PP, Newcomer ME (1997) The SH3 domain of Eps8 exists as a novel intertwined dimer. Nat Struct Biol 4:739-743.
37. Kristensen O, et al. (2006) A unique set of SH3-SH3 interactions controls IB1 homodimerization. EMBO J 22:785-797.
38. Pasqualini R, Koivunen E, Ruoslahti E (1997) Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat Biotechnol 15:542-546.
39. Takagi J, Petre BM, Walz T, Springer TA (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110:599-611.
40. Sinclair JF, O'Brien AD (2002) Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-γ of enterohemorrhagic Escherichia coli O157:H7. J Biol Chem 277:2876-2885.
41. Hovanessian AG, et al. (2000) The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp Cell Res 261:312-328.
42. Monferran S, Paupert J, Dauvillier S, Salles B, Muller C (2004) The membrane form of the DNA repair protein Ku interacts at the cell surface with metalloproteinase 9. EMBO J 23:3758-3768.
43. Shin BK, et al. (2003) Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J Biol Chem 278:7607-7616.
44. Mintz PJ, et al. (2003) Fingerprinting the circulating repertoire of antibodies from cancer patients. Nat Biotechnol 21:57-63.
45. Barker TH, et al. (2005) SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem 280:36483-36493.
46. Goldstein NI, Prewett M, Zuklys K, Rockwell P, Mendelsohn J (1995) Biological efficacy of a chimeric antibody to the epidermal growth factor receptor in a human tumor xenograft model. Clin Cancer Res 11:1311-1318.
47. Marchiò S, et al. (2004) Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 5:151-162.
48. Smith GP, Scott JK (1993) Libraries of peptides and proteins displayed on filamentous phage. Methods Enzymol 217:228-257.