Photo of Joan S. Brugge,  PhD

Joan S. Brugge, PhD

Harvard Medical School

Harvard Medical School
Phone: (617) 432-3974
Fax: (617) 432-3969


joan_brugge@hms.harvard.edu

Joan S. Brugge, PhD

Harvard Medical School

EDUCATIONAL TITLES

  • Louise Foote Pfeiffer Professor of Cell Biology, Cell Biology, Harvard Medical School
  • Chair, Cell Biology, Harvard Medical School

DF/HCC PROGRAM AFFILIATION

Research Abstract

The Brugge laboratory is investigating the cellular processes and pathways that are involved in normal morphogenesis of epithelial tissues and the initiation and progression of epithelial tumors. Currently, most of our studies involve investigations relating to breast cancer. One of the major approaches that we use to investigate these processes involves culturing breast epithelial cells reconstituted basement membrane gels which allows the cells to organize into 3-dimensional structures that resemble the hollow, spherical glandular units of the breast. This culture system allows us to model events that control the proliferation, survival and migration of normal epithelial cells, to identify cellular genes that allow escape from these controls and induce phenotypic changes resembling those associated with tumor progression, and to elucidate the mechanisms responsible for these events.

One of the major focuses of this project involves studies of cell death processes that are critically involved in the formation of a lumen in the spheroid, gland-like breast epithelial structures and how oncogenes escape these death processes to allow filling of the luminal space. One of the hallmarks of early-stage carcinomas filling of the lumen. We have found that multiple processes contribute to the death or clearance of cells from the lumen, including apoptosis, metabolic impairment and autophagy, and intercalation into the outer cell monolayer. Our studies indicate that the induction of apoptosis and autophagy may be a consequence of lack of matrix protein deposition by the inner cells of the acinar structures, so we are investigating how matrix proteins regulate apoptosis and metabolic activity and how oncogenes suppress apoptosis and allow rescue from metabolic impairment. Lastly, we have identified a novel, non-apoptotic mechanism of cell death that involves invasion of one cell into the other, followed by lysosomal degradation of the invading cell. We are exploring the role of this process in tumor surveillance and other physiological processes.

Another major focus is on cellular pathways that regulate the aberrant migration and invasion of tumor cells. We are carrying out siRNA screens to identify genes that inhibit or enhance cell migration and invasion, investigating the mechanisms responsible for these events, and establishing whether these pathways are involved in invasion in vivo.

Other studies involve investigations of cellular pathways that control normal differentiation of breast epithelial cells in order to understand the contribution of factors and pathways that regulate these events in tumorigenesis.

Publications

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  • Godinho SA, Picone R, Burute M, Dagher R, Su Y, Leung CT, Polyak K, Brugge JS, Théry M, Pellman D. Oncogene-like induction of cellular invasion from centrosome amplification. Nature 2014. PubMed
  • Davidowitz RA, Selfors LM, Iwanicki MP, Elias KM, Karst A, Piao H, Ince TA, Drage MG, Dering J, Konecny GE, Matulonis U, Mills GB, Slamon DJ, Drapkin R, Brugge JS. Mesenchymal gene program-expressing ovarian cancer spheroids exhibit enhanced mesothelial clearance. J Clin Invest 2014. PubMed
  • Ng MR, Besser A, Brugge JS, Danuser G. Mapping the dynamics of force transduction at cell-cell junctions of epithelial clusters. Elife 2015; 3:e03282. PubMed
  • Kaanta AS, Virtanen C, Selfors LM, Brugge JS, Neel BG. Evidence for a multipotent mammary progenitor with pregnancy-specific activity. Breast Cancer Res 2013; 15:R65. PubMed
  • Vakifahmetoglu-Norberg H, Kim M, Xia HG, Iwanicki MP, Ofengeim D, Coloff JL, Pan L, Ince TA, Kroemer G, Brugge JS, Yuan J. Chaperone-mediated autophagy degrades mutant p53. Genes Dev 2013; 27:1718-30. PubMed
  • Buchwalter G, Hickey MM, Cromer A, Selfors LM, Gunawardane RN, Frishman J, Jeselsohn R, Lim E, Chi D, Fu X, Schiff R, Brown M, Brugge JS. PDEF promotes luminal differentiation and acts as a survival factor for ER-positive breast cancer cells. Cancer Cell 2013; 23:753-67. PubMed
  • Mouneimne G, Hansen SD, Selfors LM, Petrak L, Hickey MM, Gallegos LL, Simpson KJ, Lim J, Gertler FB, Hartwig JH, Mullins RD, Brugge JS. Differential remodeling of actin cytoskeleton architecture by profilin isoforms leads to distinct effects on cell migration and invasion. Cancer Cell 2012; 22:615-30. PubMed
  • Ng MR, Besser A, Danuser G, Brugge JS. Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J Cell Biol 2012; 199:545-63. PubMed
  • Kim JH, Cho A, Yin H, Schafer DA, Mouneimne G, Simpson KJ, Nguyen KV, Brugge JS, Montell DJ. Psidin, a conserved protein that regulates protrusion dynamics and cell migration. Genes Dev 2011; 25:730-41. PubMed
  • Albeck JG, Brugge JS. Uncovering a tumor suppressor for triple-negative breast cancers. Cell 2011; 144:638-40. PubMed
  • Krajcovic M, Johnson NB, Sun Q, Normand G, Hoover N, Yao E, Richardson AL, King RW, Cibas ES, Schnitt SJ, Brugge JS, Overholtzer M. A non-genetic route to aneuploidy in human cancers. Nat Cell Biol 2011; 13:324-30. PubMed
  • Grassian AR, Schafer ZT, Brugge JS. ErbB2 stabilizes epidermal growth factor receptor (EGFR) expression via Erk and Sprouty2 in extracellular matrix detached cells. J Biol Chem 2011; 286:79-90. PubMed
  • Harrison SC, Brugge JS. Mechanistic biology in the next quarter century. Mol Biol Cell 2010; 21:3799-800. PubMed
  • Tushir JS, Clancy J, Warren A, Wrobel C, Brugge JS, D'Souza-Schorey C. Unregulated ARF6 Activation in Epithelial Cysts Generates Hyperactive Signaling Endosomes and Disrupts Morphogenesis. Mol Biol Cell 2010; 21:2355-66. PubMed
  • Janes KA, Wang CC, Holmberg KJ, Cabral K, Brugge JS. Identifying single-cell molecular programs by stochastic profiling. Nat Methods 2010; 7:311-7. PubMed
  • Zhou W, Hur W, McDermott U, Dutt A, Xian W, Ficarro SB, Zhang J, Sharma SV, Brugge J, Meyerson M, Settleman J, Gray NS. A structure-guided approach to creating covalent FGFR inhibitors. Chem Biol 2010; 17:285-95. PubMed
  • Mazzone M, Selfors LM, Albeck J, Overholtzer M, Sale S, Carroll DL, Pandya D, Lu Y, Mills GB, Aster JC, Artavanis-Tsakonas S, Brugge JS. Dose-dependent induction of distinct phenotypic responses to Notch pathway activation in mammary epithelial cells. Proc Natl Acad Sci U S A 2010; 107:5012-7. PubMed
  • Wolfer A, Wittner BS, Irimia D, Flavin RJ, Lupien M, Gunawardane RN, Meyer CA, Lightcap ES, Tamayo P, Mesirov JP, Liu XS, Shioda T, Toner M, Loda M, Brown M, Brugge JS, Ramaswamy S. MYC regulation of a "poor-prognosis" metastatic cancer cell state. Proc Natl Acad Sci U S A 2010; 107:3698-703. PubMed
  • Knowlton ML, Selfors LM, Wrobel CN, Gu TL, Ballif BA, Gygi SP, Polakiewicz R, Brugge JS. Profiling Y561-dependent and -independent substrates of CSF-1R in epithelial cells. PLoS ONE 2010; 5:e13587. PubMed
  • Irie HY, Shrestha Y, Selfors LM, Frye F, Iida N, Wang Z, Zou L, Yao J, Lu Y, Epstein CB, Natesan S, Richardson AL, Polyak K, Mills GB, Hahn WC, Brugge JS. PTK6 regulates IGF-1-induced anchorage-independent survival. PLoS ONE 2010; 5:e11729. PubMed
  • Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, Lukashchuk N, Gillespie DA, Ludwig RL, Gosselin P, Cromer A, Brugge JS, Sansom OJ, Norman JC, Vousden KH. Mutant p53 drives invasion by promoting integrin recycling. Cell 2010; 139:1327-41. PubMed
  • Leung CT, Brugge JS. Tumor self-seeding: bidirectional flow of tumor cells. Cell 2010; 139:1226-8. PubMed
  • Ng MR, Brugge JS. A stiff blow from the stroma: collagen crosslinking drives tumor progression. Cancer Cell 2009; 16:455-7. PubMed
  • Zhang J, Ji JY, Yu M, Overholtzer M, Smolen GA, Wang R, Brugge JS, Dyson NJ, Haber DA. YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat Cell Biol 2009; 11:1444-50. PubMed
  • Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, Gao S, Puigserver P, Brugge JS. Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 2009; 461:109-13. PubMed
  • Mouneimne G,Brugge JS. YB-1 translational control of epithelial-mesenchyme transition. Cancer Cell 2009; 15:357-9. PubMed
  • Xian W,Pappas L,Pandya D,Selfors LM,Derksen PW,de Bruin M,Gray NS,Jonkers J,Rosen JM,Brugge JS. Fibroblast growth factor receptor 1-transformed mammary epithelial cells are dependent on RSK activity for growth and survival. Cancer Res 2009; 69:2244-51. PubMed
  • Iwanicki MP, Brugge JS. Transcriptional regulation of metastatic [Id]entity by KLF17. Genome Biol 2010; 10:244. PubMed
  • Overholtzer M,Brugge JS. The cell biology of cell-in-cell structures. Nat Rev Mol Cell Biol 2008; 9:796-809. PubMed
  • Simpson KJ,Selfors LM,Bui J,Reynolds A,Leake D,Khvorova A,Brugge JS. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 2009; 10:1027-38. PubMed
  • Simpson KJ,Selfors LM,Bui J,Reynolds A,Leake D,Khvorova A,Brugge JS. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 2008. PubMed
  • Melani M, Simpson KJ, Brugge JS, Montell D. Regulation of cell adhesion and collective cell migration by hindsight and its human homolog RREB1. Curr Biol 2008; 18:532-7. PubMed
  • Mailleux AA, Overholtzer M, Brugge JS. [Entosis, a cell death process related to cell cannibalism between tumor cells] Med Sci (Paris) 2008; 24:246-8. PubMed
  • Mailleux AA, Overholtzer M, Brugge JS. Lumen formation during mammary epithelial morphogenesis: insights from in vitro and in vivo models. Cell Cycle 2008; 7:57-62. PubMed
  • Tamimi RM, Brugge JS, Freedman ML, Miron A, Iglehart JD, Colditz GA, Hankinson SE. Circulating colony stimulating factor-1 and breast cancer risk. Cancer Res 2008; 68:18-21. PubMed
  • Schafer ZT, Brugge JS. IL-6 involvement in epithelial cancers. J Clin Invest 2007; 117:3660-3. PubMed
  • Overholtzer M, Mailleux AA, Mouneimne G, Normand G, Schnitt SJ, King RW, Cibas ES, Brugge JS. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 2007; 131:966-79. PubMed
  • Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, Polverini PJ, Mooney DJ. Engineering tumors with 3D scaffolds. Nat Methods 2007; 4:855-60. PubMed
  • Mouneimne G, Brugge JS. Tensins: a new switch in cell migration. Dev Cell 2007; 13:317-9. PubMed
  • Miller-Jensen K, Janes KA, Brugge JS, Lauffenburger DA. Common effector processing mediates cell-specific responses to stimuli. Nature 2007; 448:604-8. PubMed
  • Brugge J, Hung MC, Mills GB. A new mutational AKTivation in the PI3K pathway. Cancer Cell 2007; 12:104-7. PubMed
  • Schmelzle T, Mailleux AA, Overholtzer M, Carroll JS, Solimini NL, Lightcap ES, Veiby OP, Brugge JS. Functional role and oncogene-regulated expression of the BH3-only factor Bmf in mammary epithelial anoikis and morphogenesis. Proc Natl Acad Sci U S A 2007; 104:3787-92. PubMed
  • Mailleux AA, Overholtzer M, Schmelzle T, Bouillet P, Strasser A, Brugge JS. BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 2007; 12:221-34. PubMed
  • Carroll DK, Brugge JS, Attardi LD. p63, cell adhesion and survival. Cell Cycle 2007; 6:255-61. PubMed
  • Walker SJ, Brugge JS. SePARating polarity and proliferation in ErbB2 oncogenesis. Nat Cell Biol 2006; 8:1220-2. PubMed
  • Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC, Deng CX, Brugge JS, Haber DA. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci U S A 2006; 103:12405-10. PubMed
  • Carroll DK, Carroll JS, Leong CO, Cheng F, Brown M, Mills AA, Brugge JS, Ellisen LW. p63 regulates an adhesion programme and cell survival in epithelial cells. Nat Cell Biol 2006; 8:551-61. PubMed
  • Wilsbacher JL, Moores SL, Brugge JS. An active form of Vav1 induces migration of mammary epithelial cells by stimulating secretion of an epidermal growth factor receptor ligand. Cell Commun Signal 2006; 4:5. PubMed
  • Witt AE, Hines LM, Collins NL, Hu Y, Gunawardane RN, Moreira D, Raphael J, Jepson D, Koundinya M, Rolfs A, Taron B, Isakoff SJ, Brugge JS, LaBaer J. Functional proteomics approach to investigate the biological activities of cDNAs implicated in breast cancer. J Proteome Res 2006; 5:599-610. PubMed
  • Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, Kothari N, Natesan S, Brugge JS. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol 2005; 171:1023-34. PubMed
  • Gunawardane RN, Sgroi DC, Wrobel CN, Koh E, Daley GQ, Brugge JS. Novel role for PDEF in epithelial cell migration and invasion. Cancer Res 2005; 65:11572-80. PubMed
  • Isakoff SJ, Engelman JA, Irie HY, Luo J, Brachmann SM, Pearline RV, Cantley LC, Brugge JS. Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res 2005; 65:10992-1000. PubMed
  • Yan SR, Joseph RR, Rosen K, Reginato MJ, Jackson A, Allaire N, Brugge JS, Jobin C, Stadnyk AW. Activation of NF-kappaB following detachment delays apoptosis in intestinal epithelial cells. Oncogene 2005; 24:6482-91. PubMed
  • Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005; 5:675-88. PubMed
  • Reginato MJ, Mills KR, Becker EB, Lynch DK, Bonni A, Muthuswamy SK, Brugge JS. Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol Cell Biol 2005; 25:4591-601. PubMed
  • Collins NL, Reginato MJ, Paulus JK, Sgroi DC, Labaer J, Brugge JS. G1/S cell cycle arrest provides anoikis resistance through Erk-mediated Bim suppression. Mol Cell Biol 2005; 25:5282-91. PubMed
  • Cowan CW, Shao YR, Sahin M, Shamah SM, Lin MZ, Greer PL, Gao S, Griffith EC, Brugge JS, Greenberg ME. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 2005; 46:205-17. PubMed
  • Martin SS, Ridgeway AG, Pinkas J, Lu Y, Reginato MJ, Koh EY, Michelman M, Daley GQ, Brugge JS, Leder P. A cytoskeleton-based functional genetic screen identifies Bcl-xL as an enhancer of metastasis, but not primary tumor growth. Oncogene 2004; 23:4641-5. PubMed
  • Ma XJ, Wang Z, Ryan PD, Isakoff SJ, Barmettler A, Fuller A, Muir B, Mohapatra G, Salunga R, Tuggle JT, Tran Y, Tran D, Tassin A, Amon P, Wang W, Wang W, Enright E, Stecker K, Estepa-Sabal E, Smith B, Younger J, Balis U, Michaelson J, Bhan A, Habin K, Baer TM, Brugge J, Haber DA, Erlander MG, Sgroi DC. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004; 5:607-16. PubMed
  • Mills KR, Reginato M, Debnath J, Queenan B, Brugge JS. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci U S A 2004; 101:3438-43. PubMed
  • Seton-Rogers SE, Lu Y, Hines LM, Koundinya M, LaBaer J, Muthuswamy SK, Brugge JS. Cooperation of the ErbB2 receptor and transforming growth factor beta in induction of migration and invasion in mammary epithelial cells. Proc Natl Acad Sci U S A 2004; 101:1257-62. PubMed
  • Fujikawa K, Miletic AV, Alt FW, Faccio R, Brown T, Hoog J, Fredericks J, Nishi S, Mildiner S, Moores SL, Brugge J, Rosen FS, Swat W. Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med 2003; 198:1595-608. PubMed
  • Debnath J, Walker SJ, Brugge JS. Akt activation disrupts mammary acinar architecture and enhances proliferation in an mTOR-dependent manner. J Cell Biol 2003; 163:315-26. PubMed
  • Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J, Muthuswamy SK, Brugge JS. Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol 2003; 5:733-40. PubMed
  • Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, Lugovskoy AA, Baird CL, Zhu H, Field SJ, Lessnick SL, Villasenor J, Mehrotra B, Chen J, Rao VR, Brugge JS, Ferguson CG, Payrastre B, Myszka DG, Cantley LC, Wagner G, Divecha N, Prestwich GD, Yuan J. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 2003; 114:99-111. PubMed
  • Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30:256-68. PubMed
  • Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002; 111:29-40. PubMed
  • Miranti CK, Brugge JS. Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol 2002; 4:E83-90. PubMed
  • Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001; 3:785-92. PubMed
  • Sever R, Brugge JS. Signal Transduction in Cancer. Cold Spring Harb Perspect Med 2015. PubMed
  • Muthuswamy SK, Gilman M, Brugge JS. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers. Mol Cell Biol 1999; 19:6845-57. PubMed
  • Miranti CK, Ohno S, Brugge JS. Protein kinase C regulates integrin-induced activation of the extracellular regulated kinase pathway upstream of Shc. J Biol Chem 1999; 274:10571-81. PubMed
  • Clark EA, King WG, Brugge JS, Symons M, Hynes RO. Integrin-mediated signals regulated by members of the rho family of GTPases. J Cell Biol 1998; 142:573-86. PubMed
  • Gao J, Zoller KE, Ginsberg MH, Brugge JS, Shattil SJ. Regulation of the pp72syk protein tyrosine kinase by platelet integrin alpha IIb beta 3. EMBO J 1997; 16:6414-25. PubMed
  • King WG, Mattaliano MD, Chan TO, Tsichlis PN, Brugge JS. Phosphatidylinositol 3-kinase is required for integrin-stimulated AKT and Raf-1/mitogen-activated protein kinase pathway activation. Mol Cell Biol 1997; 17:4406-18. PubMed
  • Zoller KE, MacNeil IA, Brugge JS. Protein tyrosine kinases Syk and ZAP-70 display distinct requirements for Src family kinases in immune response receptor signal transduction. J Immunol 1997; 158:1650-9. PubMed
  • Bolen JB, Brugge JS. Leukocyte protein tyrosine kinases: potential targets for drug discovery. Annu Rev Immunol 1997; 15:371-404. PubMed
  • Thomas SM, Brugge JS. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 1998; 13:513-609. PubMed
  • Cichowski K, Brugge JS, Brass LF. Thrombin receptor activation and integrin engagement stimulate tyrosine phosphorylation of the proto-oncogene product, p95vav, in platelets. J Biol Chem 1996; 271:7544-50. PubMed
  • Rusanescu G, Qi H, Thomas SM, Brugge JS, Halegoua S. Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron 1995; 15:1415-25. PubMed
  • Rickles RJ, Botfield MC, Zhou XM, Henry PA, Brugge JS, Zoller MJ. Phage display selection of ligand residues important for Src homology 3 domain binding specificity. Proc Natl Acad Sci U S A 1995; 92:10909-13. PubMed
  • Weng Z, Rickles RJ, Feng S, Richard S, Shaw AS, Schreiber SL, Brugge JS. Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol Cell Biol 1995; 15:5627-34. PubMed
  • Mukhopadhyay D, Tsiokas L, Zhou XM, Foster D, Brugge JS, Sukhatme VP. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature 1995; 375:577-81. PubMed
  • Shiue L, Zoller MJ, Brugge JS. Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J Biol Chem 1995; 270:10498-502. PubMed
  • Rivera VM, Brugge JS. Clustering of Syk is sufficient to induce tyrosine phosphorylation and release of allergic mediators from rat basophilic leukemia cells. Mol Cell Biol 1995; 15:1582-90. PubMed
  • Rickles RJ, Botfield MC, Weng Z, Taylor JA, Green OM, Brugge JS, Zoller MJ. Identification of Src, Fyn, Lyn, PI3K and Abl SH3 domain ligands using phage display libraries. EMBO J 1994; 13:5598-604. PubMed
  • Clark EA, Shattil SJ, Brugge JS. Regulation of protein tyrosine kinases in platelets. Trends Biochem Sci 1994; 19:464-9. PubMed
  • Clark EA, Trikha M, Markland FS, Brugge JS. Structurally distinct disintegrins contortrostatin and multisquamatin differentially regulate platelet tyrosine phosphorylation. J Biol Chem 1994; 269:21940-3. PubMed
  • Shattil SJ, Haimovich B, Cunningham M, Lipfert L, Parsons JT, Ginsberg MH, Brugge JS. Tyrosine phosphorylation of pp125FAK in platelets requires coordinated signaling through integrin and agonist receptors. J Biol Chem 1994; 269:14738-45. PubMed
  • Thomas JE, Aguzzi A, Soriano P, Wagner EF, Brugge JS. Induction of tumor formation and cell transformation by polyoma middle T antigen in the absence of Src. Oncogene 1993; 8:2521-9. PubMed
  • Weng Z, Taylor JA, Turner CE, Brugge JS, Seidel-Dugan C. Detection of Src homology 3-binding proteins, including paxillin, in normal and v-Src-transformed Balb/c 3T3 cells. J Biol Chem 1993; 268:14956-63. PubMed
  • Huang MM, Lipfert L, Cunningham M, Brugge JS, Ginsberg MH, Shattil SJ. Adhesive ligand binding to integrin alpha IIb beta 3 stimulates tyrosine phosphorylation of novel protein substrates before phosphorylation of pp125FAK. J Cell Biol 1993; 122:473-83. PubMed
  • Brugge JS. New intracellular targets for therapeutic drug design. Science 1993; 260:918-9. PubMed
  • Clark EA, Brugge JS. Redistribution of activated pp60c-src to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol Cell Biol 1993; 13:1863-71. PubMed
  • Yu H, Rosen MK, Shin TB, Seidel-Dugan C, Brugge JS, Schreiber SL. Solution structure of the SH3 domain of Src and identification of its ligand-binding site. Science 1992; 258:1665-8. PubMed
  • Lipfert L, Haimovich B, Schaller MD, Cobb BS, Parsons JT, Brugge JS. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125FAK in platelets. J Cell Biol 1992; 119:905-12. PubMed
  • Thomas SM, DeMarco M, D'Arcangelo G, Halegoua S, Brugge JS. Ras is essential for nerve growth factor- and phorbol ester-induced tyrosine phosphorylation of MAP kinases. Cell 1992; 68:1031-40. PubMed
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