Apoptosis and Cancer Biology


Select Publications


Selected Publications on Crk and Cancer:


  1. Cyclophilin A promotes cell migration via the Abl-Crk signaling pathway.
    Saleh T, Jankowski W, Sriram G, Rossi P, Shah S, Lee KB, Cruz LA, Rodriguez AJ, Birge RB, Kalodimos CG.
    Nat Chem Biol. 2016 Feb;12(2):117-23. doi: 10.1038/nchembio.1981.
    PMID: 26656091
  2. Reciprocal regulation of Abl kinase by Crk Y251 and Abi1 controls invasive phenotypes in glioblastoma.
    Kumar S, Lu B, Dixit U, Hossain S, Liu Y, Li J, Hornbeck P, Zheng W, Sowalsky AG, Kotula L, Birge RB.
    Oncotarget. 2015 Nov 10;6(35):37792-807. doi: 10.18632/oncotarget.6096.
    PMID: 26473374
  3. Iterative tyrosine phosphorylation controls non-canonical domain utilization in Crk.
    Sriram G, Jankowski W, Kasikara C, Reichman C, Saleh T, Nguyen KQ, Li J, Hornbeck P, Machida K, Liu T, Li H, Kalodimos CG, Birge RB.
    Oncogene. 2015 Aug 6;34(32):4260-9. doi: 10.1038/onc.2014.361.
    PMID: 25381819
  4. Crk at the quarter century mark: perspectives in signaling and cancer.
    Kumar S, Fajardo JE, Birge RB, Sriram G.
    J Cell Biochem. 2014 May;115(5):819-25. doi: 10.1002/jcb.24749.
    PMID: 24356912
  5. Crk and ABI1: binary molecular switches that regulate abl tyrosine kinase and signaling to the cytoskeleton.
    Hossain S, Dubielecka PM, Sikorski AF, Birge RB, Kotula L.
    Genes Cancer. 2012 May;3(5-6):402-13. doi: 10.1177/1947601912460051.
    PMID: 23226578
  6. Monographs editor.
    Birge RB.
    Genes Cancer. 2012 May;3(5-6):331. doi: 10.1177/1947601912460548. No abstract available.
    PMID: 23226570
  7. Commentary: The carboxyl-terminal Crk SH3 domain: Regulatory strategies and new perspectives.
    Sriram G, Birge RB.
    FEBS Lett. 2012 Aug 14;586(17):2615-8. doi: 10.1016/j.febslet.2012.04.040. Review.
    PMID: 22710158
  8. Domain organization differences explain Bcr-Abl's preference for CrkL over CrkII.
    Jankowski W, Saleh T, Pai MT, Sriram G, Birge RB, Kalodimos CG.
    Nat Chem Biol. 2012 May 13;8(6):590-6. doi: 10.1038/nchembio.954.
    PMID: 22581121
  9. Emerging roles for crk in human cancer. Sriram G, Birge RB.
    Genes Cancer. 2010 Nov;1(11):1132-9. doi: 10.1177/1947601910397188.
    PMID: 21779437
  10. Phosphorylation of Crk on Tyrosine 251 in the RT-loop of the carboxyl-terminal SH3 domain promotes Abl Kinase Trans-activation.
    G.Sriram, C.Reichman, A.Tunceroglu, N.Kaushal, T.Saleh, K.Machida, B.J.Mayer, J.Li, QingyuanGe, C.G.Kalodimos, and Birge RB.
    Oncogene. 2011 Nov 17;30(46):4645-55. doi: 10.1038/onc.2011.170.
    PMID: 21602891
  11. Structural basis for auto-inhibition and activation of the Crk oncogene protein by a proline switch.
    Sarkar P, Saleh T, Tzeng SR, Birge RB, Kalodimos CG.
    Nat Chem Biol. 2011 Jan;7(1):51-7. doi: 10.1038/nchembio.494.
    PMID: 21131971
  12. Sphingosine kinase 1 overexpression is regulated by signaling through PI3K, AKT2, and mTOR in imatinib-resistant chronic myeloid leukemia cells.
    Marfe G, Di Stefano C, Gambacurta A, Ottone T, Martini V, Abruzzese E, Mologni L, Sinibaldi-Salimei P, de Fabritis P, Gambacorti-Passerini C, Amadori S, Birge RB.
    Exp Hematol. 2011 Jun;39(6):653-665.e6. doi: 10.1016/j.exphem.2011.02.013.
    PMID: 21392556
  13. Real-time fluorescent resonance energy transfer analysis to monitor drug resistance in chronic myelogenous leukemia.
    Tunceroglu A, Matsuda M, Birge RB.
    Mol Cancer Ther. 2010 Nov;9(11):3065-73. doi: 10.1158/1535-7163.MCT-10-0623.
    PMID: 20817824
  14. Crk and CrkL adaptor proteins: networks for physiological and pathological signaling.
    Birge RB, Kalodimos C, Inagaki F, Tanaka S.
    Cell Commun Signal. 2009 May 10;7:13. doi: 10.1186/1478-811X-7-13.
    PMID: 19426560
  15. Proapoptotic function of the nuclear Crk II adaptor protein.
    Kar B, Reichman CT, Singh S, O'Connor JP, Birge RB.
    Biochemistry. 2007 Sep 25;46(38):10828-40.
    PMID: 17764157
  16. Proline cis-trans isomerization controls autoinhibition of a signaling protein.
    Sarkar P, Reichman C, Saleh T, Birge RB, Kalodimos CG.
    Mol Cell. 2007 Feb 9;25(3):413-26.
    PMID: 17289588
  17. Transactivation of Abl by the Crk II adapter protein requires a PNAY sequence in the Crk C-terminal SH3 domain.
    Reichman C, Singh K, Liu Y, Singh S, Li H, Fajardo JE, Fiser A, Birge RB.
    Oncogene. 2005 Dec 8;24(55):8187-99.
    PMID: 16158059
  18. Activation of the focal adhesion kinase signaling pathway by structural alterations in the carboxyl-terminal region of c-Crk II.
    Zvara A, Fajardo JE, Escalante M, Cotton G, Muir T, Kirsch KH, Birge RB.
    Oncogene. 2001 Feb 22;20(8):951-61.
    PMID: 11314030
  19. Activation of Rho-dependent cell spreading and focal adhesion biogenesis by the v-Crk adaptor protein.
    Altun-Gultekin ZF, Chandriani S, Bougeret C, Ishizaki T, Narumiya S, de Graaf P, Van Bergen en Henegouwen P, Hanafusa H, Wagner JA, Birge RB.
    Mol Cell Biol. 1998 May;18(5):3044-58.
    PMID: 9566923
  20. Closing in on SH2 specificity.
    Birge RB, Hanafusa H.
    Science. 1993 Dec 3;262(5139):1522-4. Review. No abstract available.
    PMID: 7504323
  21. SH2 domains recognize specific phosphopeptide sequences.
    Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ, Birge RB, et al.
    Cell. 1993 Mar 12;72(5):767-78.
    PMID: 7680959
  22. Crystal structure of the phosphotyrosine recognition domain SH2 of v-src complexed with tyrosine-phosphorylated peptides.
    Waksman G, Kominos D, Robertson SC, Pant N, Baltimore D, Birge RB, Cowburn D, Hanafusa H, Mayer BJ, Overduin M, Resh MD, Rios CB, Silverman L, Kuriyan J.
    Nature. 1992 Aug 20;358(6388):646-53.
    PMID: 1379696

Selected Publications on apoptosis and cell clearance:


  1. Ligand Activation of TAM Family Receptors-Implications for Tumor Biology and Therapeutic Response.
    Davra V, Kimani SG, Calianese D, Birge RB.
    Cancers (Basel). 2016 Nov 29;8(12). pii: E107. Review.
    PMID: 27916840
  2. Normalization of TAM post-receptor signaling reveals a cell invasive signature for Axl tyrosine kinase.
    Kimani SG, Kumar S, Davra V, Chang YJ, Kasikara C, Geng K, Tsou WI, Wang S, Hoque M, Boháč A, Lewis-Antes A, De Lorenzo MS, Kotenko SV, Birge RB.
    Cell Commun Signal. 2016 Sep 6;14(1):19. doi: 10.1186/s12964-016-0142-1.
    PMID: 27595981
  3. Efferocytosis.
    Kumar S, Birge RB.
    Curr Biol. 2016 Jul 11;26(13):R558-9. doi: 10.1016/j.cub.2016.01.059.
    PMID: 27404247
  4. Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer.
    Birge RB, Boeltz S, Kumar S, Carlson J, Wanderley J, Calianese D, Barcinski M, Brekken RA, Huang X, Hutchins JT, Freimark B, Empig C, Mercer J, Schroit AJ, Schett G, Herrmann M.
    Cell Death Differ. 2016 Jun;23(6):962-78. doi: 10.1038/cdd.2016.11. Review.
    PMID: 26915293
  5. Molecular and Translational Classifications of DAMPs in Immunogenic Cell Death.
    Garg AD, Galluzzi L, Apetoh L, Baert T, Birge RB, Bravo-San Pedro JM, Breckpot K, Brough D, Chaurio R, Cirone M, Coosemans A, Coulie PG, De Ruysscher D, Dini L, de Witte P, Dudek-Peric AM, Faggioni A, Fucikova J, Gaipl US, Golab J, Gougeon ML, Hamblin MR, Hemminki A, Herrmann M, Hodge JW, Kepp O, Kroemer G, Krysko DV, Land WG, Madeo F, Manfredi AA, Mattarollo SR, Maueroder C, Merendino N, Multhoff G, Pabst T, Ricci JE, Riganti C, Romano E, Rufo N, Smyth MJ, Sonnemann J, Spisek R, Stagg J, Vacchelli E, Vandenabeele P, Vandenberk L, Van den Eynde BJ, Van Gool S, Velotti F, Zitvogel L, Agostinis P.
    Front Immunol. 2015 Nov 20;6:588. doi: 10.3389/fimmu.2015.00588.
    PMID: 26635802
  6. Contribution of Defective PS Recognition and Efferocytosis to Chronic Inflammation and Autoimmunity.
    Kimani SG, Geng K, Kasikara C, Kumar S, Sriram G, Wu Y, Birge RB.
    Front Immunol. 2014 Nov 10;5:566. doi: 10.3389/fimmu.2014.00566. Review.
    PMID: 25426118
  7. Overexpression of MERTK receptor tyrosine kinase in epithelial cancer cells drives efferocytosis in a gain-of-function capacity.
    Nguyen KQ, Tsou WI, Calarese DA, Kimani SG, Singh S, Hsieh S, Liu Y, Lu B, Wu Y, Garforth SJ, Almo SC, Kotenko SV, Birge RB.
    J Biol Chem. 2014 Sep 12;289(37):25737-49. doi: 10.1074/jbc.M114.570838.
    PMID: 25074939
  8. Receptor tyrosine kinases, TYRO3, AXL, and MER, demonstrate distinct patterns and complex regulation of ligand-induced activation.
    Tsou WI, Nguyen KQ, Calarese DA, Garforth SJ, Antes AL, Smirnov SV, Almo SC, Birge RB, Kotenko SV.
    J Biol Chem. 2014 Sep 12;289(37):25750-63. doi: 10.1074/jbc.M114.569020.
    PMID: 25074926
  9. High molecular weight kininogen binds phosphatidylserine and opsonizes urokinase plasminogen activator receptor-mediated efferocytosis.
    Yang A, Dai J, Xie Z, Colman RW, Wu Q, Birge RB, Wu Y.
    J Immunol. 2014 May 1;192(9):4398-408. doi: 10.4049/jimmunol.1302590.
    PMID: 24688027
  10. TAM receptors in apoptotic cell clearance, autoimmunity, and cancer.
    Nguyen KQ, Tsou WI, Kotenko S, Birge RB.
    Autoimmunity. 2013 Aug;46(5):294-7. doi: 10.3109/08916934.2013.794515. Review.
    PMID: 23662598
  11. ATG proteins mediate efferocytosis and suppress inflammation in mammary involution.
    Teplova I, Lozy F, Price S, Singh S, Barnard N, Cardiff RD, Birge RB, Karantza V.
    Autophagy. 2013 Apr;9(4):459-75. doi: 10.4161/auto.23164.
    PMID: 23380905
  12. S.G. Kimani, S. Kumar, Nitu Bansal, K. Singh, V. Kholodovych, T. Comollo, Y. Peng, S. V. Kotenko, S. G. Sarafianos, J. R. Bertino, W. J. Welsh, and Birge RB. (2017). Small Molecule Ig1-Gas6 inhibitors block Gas6-inducible TAM activation and tumorigenicity. Scientific Reports (in press).
  13. C. Kasikara, S Kumar, S.G Kimani, W-I Tsou, K. Geng, V. Davra, G. Sriram,, C. Devoe, K-Q N. Nguyen, A. Antes, A. Krantz, G.Rymarczyk, A. Wilczynski, C. Empig, B. Freimark, M. Gray, K. Schlunegger, J. Hutchins, S. V. Kotenkoand Birge RB (2017). Phosphatidylserine Sensing by TAM Receptors Regulates AKT-dependent Chemoresistance and PD-L1 Expression Molecular Cancer Research (in press).
  14. Externalized glycolytic enzymes are novel, conserved, and early biomarkers of apoptosis.
    Ucker DS, Jain MR, Pattabiraman G, Palasiewicz K, Birge RB, Li H.
    J Biol Chem. 2012 Mar 23;287(13):10325-43. doi: 10.1074/jbc.M111.314971.
    PMID: 22262862
  15. Apoptosis: conserved roles for integrins in clearance.
    D'mello V, Birge RB.
    Curr Biol. 2010 Apr 13;20(7):R324-7. doi: 10.1016/j.cub.2010.02.043.
    PMID: 20392425
  16. The urokinase plasminogen activator receptor promotes efferocytosis of apoptotic cells.
    D'mello V, Singh S, Wu Y, Birge RB.
    J Biol Chem. 2009 Jun 19;284(25):17030-8. doi: 10.1074/jbc.M109.010066.
    PMID: 19383607
  17. Regeneration after death: Vav3 to the rescue.
    D'mello V, Birge RB.
    Blood. 2009 May 21;113(21):5037-8. doi: 10.1182/blood-2009-02-203265. No abstract available.
    PMID: 19470433
  18. Transglutaminase 2 is needed for the formation of an efficient phagocyte portal in macrophages engulfing apoptotic cells.
    Tóth B, Garabuczi E, Sarang Z, Vereb G, Vámosi G, Aeschlimann D, Blaskó B, Bécsi B, Erdõdi F, Lacy-Hulbert A, Zhang A, Falasca L, Birge RB, Balajthy Z, Melino G, Fésüs L, Szondy Z.
    J Immunol. 2009 Feb 15;182(4):2084-92. doi: 10.4049/jimmunol.0803444.
    PMID: 19201861
  19. Autophosphorylation docking site Tyr-867 in Mer receptor tyrosine kinase allows for dissociation of multiple signaling pathways for phagocytosis of apoptotic cells and down-modulation of lipopolysaccharide-inducible NF-kappaB transcriptional activation.
    Tibrewal N, Wu Y, D'mello V, Akakura R, George TC, Varnum B, Birge RB.
    J Biol Chem. 2008 Feb 8;283(6):3618-27.
    PMID: 18039660
  20. Innate apoptotic immunity: the calming touch of death.
    Birge RB, Ucker DS.
    Cell Death Differ. 2008 Jul;15(7):1096-102. doi: 10.1038/cdd.2008.58. Review.
    PMID: 18451871
  21. A NPxY-independent beta5 integrin activation signal regulates phagocytosis of apoptotic cells.
    Singh S, D'mello V, van Bergen en Henegouwen P, Birge RB.
    Biochem Biophys Res Commun. 2007 Dec 21;364(3):540-8.
    PMID: 17963729
  22. The presumptive phosphatidylserine receptor is dispensable for innate anti-inflammatory recognition and clearance of apoptotic cells.
    Mitchell JE, Cvetanovic M, Tibrewal N, Patel V, Colamonici OR, Li MO, Flavell RA, Levine JS, Birge RB, Ucker DS.
    J Biol Chem. 2006 Mar 3;281(9):5718-25.
    PMID: 16317002
  23. Phosphatidylserine recognition by phagocytes: a view to a kill.
    Wu Y, Tibrewal N, Birge RB.
    Trends Cell Biol. 2006 Apr;16(4):189-97. Review.
    PMID: 16529932
  24. A role for Mer tyrosine kinase in alphavbeta5 integrin-mediated phagocytosis of apoptotic cells.
    Wu Y, Singh S, Georgescu MM, Birge RB.
    J Cell Sci. 2005 Feb 1;118(Pt 3):539-53.
    PMID: 15673687
  25. C-terminal SH3 domain of CrkII regulates the assembly and function of the DOCK180/ELMO Rac-GEF.
    Akakura S, Kar B, Singh S, Cho L, Tibrewal N, Sanokawa-Akakura R, Reichman C, Ravichandran KS, Birge RB.
    J Cell Physiol. 2005 Jul;204(1):344-51.
    PMID: 15700267
  26. C-terminal SH3 domain of CrkII regulates the assembly and function of the DOCK180/ELMO Rac-GEF.
    Akakura S, Kar B, Singh S, Cho L, Tibrewal N, Sanokawa-Akakura R, Reichman C, Ravichandran KS, Birge RB.
    J Cell Physiol. 2005 Jul;204(1):344-51.
    PMID: 15700267
  27. The opsonin MFG-E8 is a ligand for the alphavbeta5 integrin and triggers DOCK180-dependent Rac1 activation for the phagocytosis of apoptotic cells.
    Akakura S, Singh S, Spataro M, Akakura R, Kim JI, Albert ML, Birge RB.
    Exp Cell Res. 2004 Jan 15;292(2):403-16.
    PMID: 14697347
  28. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells.
    Albert ML, Kim JI, Birge RB.
    Nat Cell Biol. 2000 Dec;2(12):899-905.
    PMID: 11146654