erbB3 is an active tyrosine kinase capable of homo- and heterointeractions

Molecular and Cellular Biology

Volumn 34, Issue 6, 2014, Pages 965-977

  Steinkamp, Mara P ^a,b   Low Nam, Shalini T ^a,c   Yang, Shujie ^a,d   Lidke, Keith A ^b   Lidke, Diane S ^a,b   Wilson, Bridget S ^a,b  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c SOUTH DAKOTA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINE; CELL LINE, TUMOR; CHO CELLS; CRICETULUS; HUMANS; LIGANDS; MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN-TYROSINE KINASES; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84894239521     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01605-13     Document Type: Article

References (60)

1. Sithanandam G, Anderson LM. 2008. The ErbB3 receptor in cancer and cancer gene therapy. Cancer Gene Ther. 15:413-448. http://dx.doi.org/10.1038/cgt.2008.15.
2. Baselga J, Swain SM. 2009. Novel anticancer targets: revisiting ErbB2 and discovering ErbB3. Nat. Rev. Cancer 9:463-475. http://dx.doi.org/10.1038/nrc2656.
3. Guy PM, Platko JV, Cantley LC, Cerione RA, Carraway KL III. 1994. Insect cell-expressed p180 erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. U. S. A. 91:8132-8136. http://dx.doi.org/10.1073/pnas.91.17.8132.
4. Sierke SL, Cheng K, Kim HH, Koland JG. 1997. Biochemical characterization of the protein tyrosine kinase homology domain of the ErbB3 (HER3) receptor protein. Biochem. J. 322(Pt 3):757-763.
5. Yarden Y, Sliwkowski MX. 2001. Untangling the ErbB signaling network. Nat. Rev. Mol. Cell. Biol. 2:127-137. http://dx.doi.org/10.1038/35052073.
6. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, Lavi S, Seger R, Ratzkin BJ, Sela M, Yarden Y. 1996. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J. 15:2452-2467.
7. Sliwkowski MX, Schaefer G, Akita RW, Lofgren JA, Fitzpatrick VD, Nuijens A, Fendly BM, Cerione RA, Vandlen RL, Carraway KL III. 1994. Coexpression of erbB2 and erbB3 proteins reconstitutes a highaffinity receptor for heregulin. J. Biol. Chem. 269:14661-14665.
8. Ferguson KM, Darling PJ, Mohan MJ, Macatee TL, Lemmon MA. 2000. Extracellular domains drive homo- but not hetero-dimerization of erbB receptors. EMBO J. 19:4632-4643. http://dx.doi.org/10.1093/emboj/19.17.4632.
9. Riese DJ, II, van Raaij TM, Plowman GD, Andrews GC, Stern DF. 1995. The cellular response to neuregulins is governed by complex interactions of the erbB receptor family. Mol. Cell. Biol. 15:5770-5776.
10. Berger MB, Mendrola JM, Lemmon MA. 2004. ErbB3/HER3 does not homodimerize upon neuregulin binding at the cell surface. FEBS Lett. 569:332-336. http://dx.doi.org/10.1016/j.febslet.2004.06.014.
11. Bublil EM, Pines G, Patel G, Fruhwirth G, Ng T, Yarden Y. 2010. Kinase-mediated quasi-dimers of EGFR. FASEB J. 24:4744-4755. http://dx.doi.org/10.1096/fj.10-166199.
12. Shi F, Telesco SE, Liu Y, Radhakrishnan R, Lemmon MA. 2010. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc. Natl. Acad. Sci. U. S. A. 107:7692-7697. http://dx.doi.org/10.1073/pnas.1002753107.
13. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S, Chaudhuri S, Pujara K, Guillory J, Edgar KA, Janakiraman V, Scholz R-P, Bowman K, Lorenzo M, Li H, Wu J, Yuan W, Peters BA, Kan Z, Stinson J, Mak M, Modrusan Z, Eigenbrot C, Firestein R, Stern HM, Rajalingam K, Schaefer G, Merchant MA, Sliwkowski MX, de Sauvage FJ, Seshagiri S. 2013. Oncogenic ERBB3 mutations in human cancers. Cancer Cell 23:603-617. http://dx.doi.org/10.1016/j.ccr.2013.04.012.
14. Telesco SE, Shih AJ, Jia F, Radhakrishnan R. 2011. A multiscale modeling approach to investigate molecular mechanisms of pseudokinase activation and drug resistance in the HER3/ErbB3 receptor tyrosine kinase signaling network. Mol. Biosyst. 7:2066-2080. http://dx.doi.org/10.1039/c0mb00345j.
15. Lidke DS, Nagy P, Heintzmann R, Arndt-Jovin DJ, Post JN, Grecco HE, Jares-Erijman EA, Jovin TM. 2004. Quantum dot ligands provide new insights into erbB/HER receptor-mediated signal transduction. Nat. Biotechnol. 22:198-203. http://dx.doi.org/10.1038/nbt929.
16. Andrews NL, Lidke KA, Pfeiffer JR, Burns AR, Wilson BS, Oliver JM, Lidke DS. 2008. Actin restricts Fc[epsiv]RI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell Biol. 10:955-963. http://dx.doi.org/10.1038/ncb1755.
17. Andrews NL, Pfeiffer JR, Martinez AM, Haaland DM, Davis RW, Kawakami T, Oliver JM, Wilson BS, Lidke DS. 2009. Small, mobile FceRI receptor aggregates are signaling competent. Immunity 31:469-479. http://dx.doi.org/10.1016/j.immuni.2009.06.026.
18. Low-Nam ST, Lidke KA, Cutler PJ, Roovers RC, van Bergen en Henegouwen PM, Wilson BS, Lidke DS. 2011. ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nat. Struct. Mol. Biol. 18:1244-1249. http://dx.doi.org/10.1038/nsmb.2135.
19. Yang S, Raymond-Stintz MA, Ying W, Zhang J, Lidke DS, Steinberg SL, Williams L, Oliver JM, Wilson BS. 2007. Mapping ErbB receptors on breast cancer cell membranes during signal transduction. J. Cell Sci. 120:2763-2773. http://dx.doi.org/10.1242/jcs.007658.
20. Schulze WX, Deng L, Mann M. 2005. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 1:1-13. http://dx.doi.org/10.1038/msb4100012.
21. Hynes NE, Lane HA. 2005. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 5:341-354. http://dx.doi.org/10.1038/nrc1609.
22. Shankaran H, Wiley HS, Resat H. 2006. Modeling the effects of HER/ErbB1-3 coexpression on receptor dimerization and biological response. Biophys. J. 90:3993-4009. http://dx.doi.org/10.1529/biophysj.105.080580.
23. Hsieh MY, Yang S, Raymond-Stinz MA, Steinberg S, Vlachos DG, Shu W, Wilson B, Edwards JS. 2008. Stochastic simulations of ErbB homo and heterodimerisation: potential impacts of receptor conformational state and spatial segregation. IET Syst. Biol. 2:256-272. http://dx.doi.org/10.1049/iet-syb:20070073.
24. Schoeberl B, Pace EA, Fitzgerald JB, Harms BD, Xu L, Nie L, Linggi B, Kalra A, Paragas V, Bukhalid R, Grantcharova V, Kohli N, West KA, Leszczyniecka M, Feldhaus MJ, Kudla AJ, Nielsen UB. 2009. Therapeutically targeting ErbB3: a key node in ligand-induced activation of the ErbB receptor-PI3K axis. Sci. Signal. 2:ra31. http://dx.doi.org/10.1126/scisignal2000352.
25. Zhang Y, Opresko L, Shankaran H, Chrisler WB, Wiley HS, Resat H. 2009. HER/ErbB receptor interactions and signaling patterns in human mammary epithelial cells.BMCCell Biol. 10:78. http://dx.doi.org/10.1186/1471-2121-10-78.
26. Faratian D, Goltsov A, Lebedeva G, Sorokin A, Moodie S, Mullen P, Kay C, Um IH, Langdon S, Goryanin I, Harrison DJ. 2009. Systems biology reveals new strategies for personalizing cancer medicine and confirms the role of PTEN in resistance to trastuzumab. Cancer Res. 69:6713-6720. http://dx.doi.org/10.1158/0008-5472.CAN-09-0777.
27. Chen WW, Schoeberl B, Jasper PJ, Niepel M, Nielsen UB, Lauffenburger DA, Sorger PK. 2009. Input-output behavior of ErbB signaling pathways as revealed by a mass action model trained against dynamic data. Mol. Syst. Biol. 5:239. http://dx.doi.org/10.1038/msb.2008.74.
28. Lazzara MJ, Lauffenburger DA. 2009. Quantitative modeling perspectives on the ErbB system of cell regulatory processes. Exp. Cell Res. 315:717-725. http://dx.doi.org/10.1016/j.yexcr.2008.10.033.
29. Smith CS, Joseph N, Rieger B, Lidke KA. 2010. Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods 7:373-375. http://dx.doi.org/10.1038/nmeth.1449.
30. Forney GD. 1973. The Viterbi algorithm. Proc. IEEE 61:268-278. http://dx.doi.org/10.1109/PROC.1973.9030.
31. Fabian MA, WHBiggs 3rd, Treiber DK, Atteridge CE, Azimioara MD, Benedetti MG, Carter TA, Ciceri P, Edeen PT, Floyd M, Ford JM, Galvin M, Gerlach JL, Grotzfeld RM, Herrgard S, Insko DE, Insko MA, Lai AG, Lelias JM, Mehta SA, Milanov ZV, Velasco AM, Wodicka LM, Patel HK, Zarrinkar PP, Lockhart DJ. 2005. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23:329-336. http://dx.doi.org/10.1038/nbt1068.
32. Honegger AM, Dull TJ, Felder S, Van Obberghen E, Bellot F, Szapary D, Schmidt A, Ullrich A, Schlessinger J. 1987. Point mutation at the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing. Cell 51:199-209. http://dx.doi.org/10.1016/0092-8674(87)90147-4.
33. Qian X, LeVea CM, Freeman JK, Dougall WC, Greene MI. 1994. Heterodimerization of epidermal growth factor receptor and wild-type or kinase-deficient Neu: a mechanism of inter-receptor kinase activation and transphosphorylation. Proc. Natl. Acad. Sci. U. S. A. 91:1500-1504. http://dx.doi.org/10.1073/pnas.91.4.1500.
34. Chen WS, Lazar CS, Poenie M, Tsien RY, Gill GN, Rosenfeld MG. 1987. Requirement for intrinsic protein tyrosine kinase in the immediate and late actions of the EGF receptor. Nature 328:820-823. http://dx.doi.org/10.1038/328820a0.
35. Wallasch C, Weiss FU, Niederfellner G, Jallal B, Issing W, Ullrich A. 1995. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO J. 14:4267-4275.
36. Citri A, Skaria KB, Yarden Y. 2003. The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp. Cell Res. 284:54-65. http://dx.doi.org/10.1016/S0014-4827(02)00101-5.
37. Franklin MC, Carey KD, Vajdos FF, Leahy DJ, de Vos AM, Sliwkowski MX. 2004. Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex. Cancer Cell 5:317-328. http://dx.doi.org/10.1016/S1535-6108(04)00083-2.
38. Adams CW, Allison DE, Flagella K, Presta L, Clarke J, Dybdal N, McKeever K, Sliwkowski MX. 2006. Humanization of a recombinant monoclonal antibody to produce a therapeutic HER dimerization inhibitor, pertuzumab. Cancer Immunol. Immunother. 55:717-727. http://dx.doi.org/10.1007/s00262-005-0058-x.
39. Scaltriti M, Verma C, Guzman M, Jimenez J, Parra JL, Pedersen K, Smith DJ, Landolfi S, Ramon y Cajal S, Arribas J, Baselga J. 2009. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene 28:803-814. http://dx.doi.org/10.1038/onc.2008.432.
40. Hagen GM, Caarls W, Lidke KA, De Vries AH, Fritsch C, Barisas BG, Arndt-Jovin DJ, Jovin TM. 2009. Fluorescence recovery after photobleaching and photoconversion in multiple arbitrary regions of interest using a programmable array microscope. Microsc. Res. Technol. 72:431-440. http://dx.doi.org/10.1002/jemt.20686.
41. Jura N, Shan Y, Cao X, Shaw DE, Kuriyan J. 2009. Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3. Proc. Natl. Acad. Sci. U. S. A. 106:21608-21613. http://dx.doi.org/10.1073/pnas.0912101106.
42. Lidke DS, Lidke KA, Rieger B, Jovin TM, Arndt-Jovin DJ. 2005. Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J. Cell Biol. 170:619-626. http://dx.doi.org/10.1083/jcb.200503140.
43. Dietrich C, Yang B, Fujiwara T, Kusumi A, Jacobson K. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82:274-284. http://dx.doi.org/10.1016/S0006-3495(02)75393-9.
44. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T. 2005. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34:351-378. http://dx.doi.org/10.1146/annurev.biophys.34.040204.144637.
45. Macdonald-Obermann JL, Piwnica-Worms D, Pike LJ. 2012. Mechanics of EGF receptor/ErbB2 kinase activation revealed by luciferase fragment complementation imaging. Proc. Natl. Acad. Sci. U. S. A. 109:137-142. http://dx.doi.org/10.1073/pnas.1111316109.
46. Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM. 2006. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc. Natl. Acad. Sci. U. S. A. 103:18992-18997. http://dx.doi.org/10.1073/pnas.0609009103.
47. Warren CM, Landgraf R. 2006. Signaling through ErbB receptors: multiple layers of diversity and control. Cell. Signal. 18:923-933. http://dx.doi.org/10.1016/j.cellsig.2005.12.007.
48. Tzahar E, Waterman H, Chen X, Levkowitz G, Karunagaran D, Lavi S, Ratzkin BJ, Yarden Y. 1996. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16:5276-5287.
49. Tao R-H, Maruyama IN. 2008. All EGF(ErbB) receptors have preformed homo- and heterodimeric structures in living cells. J. Cell Sci. 121:3207-3217. http://dx.doi.org/10.1242/jcs.033399.
50. Alimandi M, Wang LM, Bottaro D, Lee CC, Kuo A, Frankel M, Fedi P, Tang C, Lippman M, Pierce JH. 1997. Epidermal growth factor and betacellulin mediate signal transduction through coexpressed ErbB2 and ErbB3 receptors. EMBO J. 16:5608-5617. http://dx.doi.org/10.1093/emboj/16.18.5608.
51. Margadant C, Monsuur HN, Norman JC, Sonnenberg A. 2011. Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23:607-614. http://dx.doi.org/10.1016/j.ceb.2011.08.005.
52. Zhang X, Gureasko J, Shen K, Cole PA, Kuriyan J. 2006. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125:1137-1149. http://dx.doi.org/10.1016/j.cell.2006.05.013.
53. Collier TS, Diraviyam K, Monsey J, Shen W, Sept D, Bose R. 2013. Carboxyl group footprinting mass spectrometry and molecular dynamics identify key interactions in the HER2-HER3 receptor tyrosine kinase interface. J. Biol. Chem. 288:25254-25264. http://dx.doi.org/10.1074/jbc.M113.474882.
54. Lu C, Mi LZ, Grey MJ, Zhu J, Graef E, Yokoyama S, Springer TA. 2010. Structural evidence for loose linkage between ligand binding and kinase activation in the epidermal growth factor receptor. Mol. Cell. Biol. 30:5432-5443. http://dx.doi.org/10.1128/MCB.00742-10.
55. Lidke K, Rieger B, Jovin T, Heintzmann R. 2005. Super-resolution by localization of quantum dots using blinking statistics. Opt. Express 13:7052-7062. http://dx.doi.org/10.1364/OPEX.13.007052.
56. Zhang Q, Park E, Kani K, Landgraf R. 2012. Functional isolation of activated and unilaterally phosphorylated heterodimers of ErbB2 and ErbB3 as scaffolds in ligand-dependent signaling. Proc. Natl. Acad. Sci. U. S. A. 109:13237-13242. http://dx.doi.org/10.1073/pnas.1200105109.
57. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. 1997. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16:1647-1655. http://dx.doi.org/10.1093/emboj/16.7.1647.
58. Kancha RK, von Bubnoff N, Peschel C, Duyster J. 2009. Functional analysis of epidermal growth factor receptor (EGFR) mutations and potential implications for EGFR targeted therapy. Clin. Cancer Res. 15:460-467. http://dx.doi.org/10.1158/1078-0432.CCR-08-1757.
59. Kani K, Warren CM, Kaddis CS, Loo JA, Landgraf R. 2005. Oligomers of ERBB3 have two distinct interfaces that differ in their sensitivity to disruption by heregulin. J. Biol. Chem. 280:8238-8247.
60. Landgraf R, Eisenberg D. 2000. Heregulin reverses the oligomerization of HER3. Biochemistry 39:8503-8511. http://dx.doi.org/10.1021/bi000953+.