Research

Research in the Ballif lab is primarily focused on elucidating molecular mechanisms of signal transduction with two major emphases: (A) genetically-defined signaling pathways regulating mammalian brain development and (B) core signaling pathways regulating cell proliferation, growth and survival. In addition to biochemical and cell biological approaches, we employ mass spectrometry-based proteomics as a primary tool to simultaneously monitor hundreds to thousands of proteins, their modifications and their interactions with other proteins following acute signal administration or across developmental stages.
A second focus of our work involves developing and applying proteomic methodology to advance diverse lines of biological inquiry, some of which have had little to no interface with proteomics. This makes these projects both exciting and challenging. These collaborative projects range from the identification of novel human blood group antigens; to the identification of host proteins that interact with arenavirus proteins; to targeted proteomic characterizations of wasps, pitcher plant ecosystems, ants, fruit flies, unicellular ciliates and parasitic protozoa.

Publications:

Proteomic and Signaling Studies of the Brain or Cell Migration:

• Bior K. Bior and BA Ballif. Dab1 stabilizes its interaction with Cin85 by suppressing Cin85 phosphorylation at serine 587. FEBS Letters. In Press.
• T Goswami, X Li, AM Smith, EM Luderowski, JJ Vincent, J Rush and BA Ballif. Comparative Phosphoproteomic Analysis of Neonatal and Adult Murine Brain. Proteomics.2012, 12:2185-9. Abstract
• Cheerathodi M,Ballif BA. Identification of CrkL-SH3 binding proteins from embryonic murine brain: Implications for Reelin signaling during brain development. Journal of Proteome Research. 2011, 10:4453-62. Abstract
• T Goswami and BA Ballif. "Methods for the Isolation of Phosphoproteins and Phosphopeptides for Mass Spectrometry Analysis: Toward Increased Functional Phosphoproteomics" Chapter 29 in Sample Preparation in Biological Mass Spectrometry. Springer Press. A. Ivanov and A.Lazarev,(Eds.). 2011. Link.
• Mendoza MC,Zhang W,Er EE,Ballif BA,Elliott HL,Danuser G andBlenis J. ERK-MAPK Drives Lamellipodia Protrusion by Activating the WAVE2 Regulatory Complex. Molecular Cell. 2011, 41:661-71. Abstract
• Schalm SS, Ballif BA, Buchanan SM, Phillips GR, Maniatis T. Phosphorylation of protocadherin proteins by the receptor tyrosine kinase Ret.Proceedings of the National Academy of Sciences USA. 2010,107:13894-9. Abstract
• GR Buel, J Rush, BA Ballif, Fyn promotes phosphorylation of collapsin response mediator protein 1 at tyrosine 504, a novel, isoform-specific regulatory site. Journal of Cellular Biochemistry. 2010, 111:20-8.Abstract
• BA Ballif, GR Carey, S Sunyaev, SP Gygi, Large-Scale Identification and Evolution Indexing of Tyrosine Phosphorylation Sites from Murine Brain. Journal of Proteome Research, 2008, 7:311-8.Abstract
• EC Connors, BA Ballif, AD Morielli. Homeostatic regulation of kv1.2 postassium channel trafficking by cyclic AMP. Journal of Biological Chemistry. 2008, 283:3445-53. Abstract
• MD Zappaterra, SN Lisgo, S Lindsay, SP Gygi, CA Walsh and BA Ballif. A Comparative Proteomic Analysis of Human and Rat Embryonic Cerebrospinal Fluid. Journal of Proteome Research, 2007, 6:3537-48. Abstract
• BA Ballif, Z Cao, D Schwartz, K Carraway III and SP Gygi. Identification of 14-3-3epsilon Substrates from Embryonic Murine Brain. Journal of Proteome Research, 2006, 5:2372-79. Abstract
• J Li, BA Ballif, AM Powelka, J Dai, SP Gygi and V Hsu. Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin ß1 to control cell migration. Developmental Cell, 2005, 9:1-11. Abstract
• BA Ballif, J Villén, SA Beausoleil, D Schwartz and SP Gygi. Phosphoproteomic analysis of the developing mouse brain. Molecular and Cellular Proteomics, 2004, 3:1093-101. Abstract
• BA Ballif, L Arnaud, WT Arthur, D Guris, A Imamoto and JA Cooper. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Current Biology, 2004,14:606-10. Abstract
• L Arnaud, BA Ballif and JA Cooper. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Molecular and Cellular Biology, 2003, 23:9293-302. Abstract
• BA Ballif, L Arnaud and JA Cooper. Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Research Molecular Brain Research, 2003, 117:152-9. Abstract
• L Arnaud, BA Ballif and JA Cooper. Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Current Biology, 2003, 13:9-17. Abstract

Signaling Studies in Cell Survival / DNA Damage / Cell Growth and Proliferation

• Anjum R, Pae E, Blenis J and Ballif BA. TPCK inhibits AGC kinases by direct activation loop adduction at phenylalanine-directed cysteine residues. FEBS Letters. 2012, 586(19):3471-6. Abstract
• Saha M, Carriere A, Cheerathodi M, Zhang X, Lavoie G, Rush J, Roux PP, Ballif BA. RSK phosphorylates SOS1 creating 14-3-3 docking sites and negatively regulating MAPK activation. Biochemical Journal. 2012, 447(1):159-66. Abstract
• Caldwell G, Howe A, Nickl C,; Dostmann W, Ballif BA, Deming P. Direct modulation of the protein kinase A catalytic subunit α by growth factor receptor tyrosine kinases. Journal of Cellular Biochemistry. 2012, 113(1):39-48. Abstract
• 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 26;5(10):e13587. Abstract
• Roberts-Galbraith RH, Ohi MD, Ballif BA, Chen JS, McLeod I, McDonald WH, Gygi SP, Yates JR 3rd, Gould KL.Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Molecular Cell. 2010 Jul 9;39(1):86-99. Abstract
• Foster KG,Acosta-Jaquez HA, Romeo Y, Ekim B, Soliman GA, Carriere A, Roux PP, Ballif BA, Fingar DC. Regulation of mTOR complex 1 (mTORC1) by raptor S863 and multi-site phosphorylation. Journal of Biological Chemistry. 2010.285(1):80-94. Abstract
• Acosta-Jaquez HA, Keller JA, Foster KG, Ekim B, Soliman GA, Feener EP, Ballif BA, Fingar DC. Site-specific mTOR phosphorylation promotes mTORC1-mediated signaling and cell growth.Molecular and Cellular Biology. 2009,29:4308-24. Abstract
• Deng M, Li F, Ballif BA, Li S, Chen X, Guo L, Ye X. Identification and functional analysis of a novel cyclin e/cdk2 substrate ankrd17. Journal of Biological Chemistry. 2009,284:7875-88. Abstract
• Yoon SO, Shin S, Liu Y, Ballif BA, Woo MS, Gygi SP, Blenis J. Ran-binding protein 3 phosphorylation links the Ras and PI3-kinase pathways to nucleocytoplasmic transport. Molecular Cell. 2008,29:362-75. Abstract
• S Matsuoka, BA Ballif, A Smogorzewska, ER McDonald 3rd, KE Hurov, J Luo, CE Bakalarski, Z Zhao, N Solimini, Y Lerenthal, Y Shiloh, SP Gygi, SJ Elledge. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 2007, 316:1160-6. Abstract
• B Wang, S Matsuoka, BA Ballif, D Zhang, A Smogorzewska, SP Gygi, and SJ Elledge. Abraxas and Rap80 form a novel BRCA1 protein complex required for the DNA damage response. Science, 2007, 316:1194-8. Abstract
• A Smogorzewska, S Matsuoka, P Vinciguerra, ER McDonald 3rd, KE Hurov, J Luo J, BA Ballif, SP Gygi, K Hofmann, AD D'Andrea, SJ Elledge. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell, 2007, 129:289-301. Abstract
• MK Holz, BA Ballif, SP Gygi, and J Blenis. mTOR and S6K1 mediate assembly of the translation pre-initiation complex through dynamic protein:protein interchange and ordered protein phosphorylation events. Cell, 2005, 123:569-80. Abstract
• R Anjum, PP Roux, BA Ballif, SP Gygi and J Blenis. The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Current Biology, 2005, 15:1762-7. Abstract
• BA Ballif*, PP Roux*, SA Gerber, JP MacKeigan, J Blenis and SP Gygi. Quantitative phosphorylation profiling of the ERK/p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors. Proceedings of the National Academy of Sciences USA, 2005,102:667-72. *Equal Contribution Abstract
• PP Roux, BA Ballif, R Anjum, SP Gygi and J Blenis. Tumor promoting phorbol esters and activated Ras inactivate the Tuberous Sclerosis Tumor Suppressor Complex via RSK.Proceedings of the National Academy of Sciences USA, 2004, 101:13489-94. Abstract
• CJ Richardson, M Bröenstrup, DC Fingar, K Jülich, BA Ballif, SP Gygi and J Blenis. SKAR is a specific target of S6 kinase 1 in cell growth control. Current Biology, 2004, 14:1540-9. Abstract
• BA Ballif and JBlenis. Molecular mechanisms mediating mammalian MEK-MAP Kinase cell survival signals. Cell Growth and Differentiation, 2001, 12:397-408. Abstract
• BA Ballif, A Shimamura, E Pae and J Blenis. Disruption of 3-Phosphoinositide Dependent Kinase 1 (PDK1) signaling by the anti-tumorigenic and anti-proliferative agent N-alpha-tosyl-L-phenylalanyl Chloromethyl Ketone. Journal of Biological Chemistry, 2001, 276:12466-75. Abstract
• A Shimamura*, BA Ballif*, SA Richards and J Blenis. RSK1 mediates a MEK-MAPK cell survival signal. Current Biology, 2000, 10:127-35. *Equal Contribution Abstract

Immunobiology / Immunocompatibility / Transfusion Science

• Saison C, Helias V, Ballif BA, Peyrard T, Puy H, Miyazaki T, Perrot S, Vayssier-Taussat M, Waldner M, Le Pennec PY, Cartron JP, Arnaud L. Null alleles of ABCG2 encoding the breast cancer resistance protein define the new blood group system Junior. Nature Genetics, 2012, 44:174-7. Abstract
• Helias V, Saison C, Ballif BA, Peyrard T, Takahashi J, Takahashi H, Tanaka M, Deybach JC, Puy H, Le Gall M, Sureau C, Pham BN, Le Pennec PY, Tani Y, Cartron JP, Arnaud L. ABCB6 is dispensable for erythropoiesis and specifies the new blood group system Langereis. Nature Genetics, 2012, 44:170-3. Abstract
• Saison C, Peyrard T, Landre C, Ballif BA, Schlosser KA, Dettori I, Chicheportiche P, Nemeth P, Cartron JP and Arnaud L. A new AQP1 null allele identified in a Gypsy woman who developed an anti-CO3 during her first pregnancy. Vox Sanguinus. 2012, 103:137-44. Abstract
• AT Heaslip, JM Leungl, KL Careyl, F Catti, DM Warshaw, NJ Westwood, BA Ballif, and GE Ward. A small-molecule inhibitor of T. gondii motility and invasion induces the posttranslational modification of myosin light chain-1 and inhibits parasite myosin motor activity. PLOS Pathogens. PLoS Pathogens. 2010 Jan 15;6(1):e1000720. Abstract
• BA Ballif, NV Mincek, JT Barret, ML Wilson and DL Simmons. Interaction of Cyclooxygenases-1 and -2 with an apoptosis and autoimmunity-associated protein.Proceedings of the National Academy of Sciences, USA, 1996, 93:5544-49. Abstract

Proteomic / Protein Studies in Evolution and Ecology

• Gotelli NJ, Ellison AM, Ballif BA. Environmental proteomics, biodiversity statistics and food-web structure. Trends in Ecology and Evolution. 2012, 27:436-42. Abstract
• NJ Gotelli, AM Smith, AM. Ellison and BA Ballif. Proteomic Characterization of the Major Arthropod Associates of the Carnivorous Pitcher Plant Sarracenia purpurea. Proteomics. 2011, 11:2354-8. Abstract
• Roskens VA, Carpenter JM, Pickett KM, Ballif BA.Preservation of field samples for enzymatic and proteomic characterization: analysis of proteins from the trophallactic fluid of hornets and yellowjackets. Journal of Proteome Research. 2010, 9:5484-91. Abstract

Additional Diverse Proteomic / Protein Studies

• Yano J, Rajendran A, Valentine MS, Saha M, Ballif BA, Van Houten JL. Proteomic
  analysis of the cilia membrane of Paramecium tetraurelia. Journal of Proteomics.In Press. Abstract
• Wallis JM, Borg ZD, Daly AB, Deng B, Ballif BA, Allen GB, Jaworski DM, Weiss D. Comparative Assessment of Detergent-Based Protocols for Mouse Lung De-Cellularization and Re-Cellularization.Tissue Engineering (Part C) Methods. 2012, 18:420-32. Abstract
• Daly AB, Wallis JM, Borg ZD, Bonvillain RW, Deng B, Ballif BA, Jaworski DM, Allen GB, Weiss D. Initial Binding and Re-Cellularization of De-Cellularized Mouse Lung Scaffolds with Bone Marrow-Derived Mesenchymal Stromal Cells. Tissue Engineering. (Part A). 2011.18:1-16. Abstract
• Purmessur D, Schek RM, Abbott RD, Ballif BA, Godburn KE and Iatridis JC. Notochordal tissue increases proteoglycan accumulation and promotes a healthy nucleus pulposus phenotype in human MSCs. Arthritis Research & Therapy. 2011. 13:R81. Abstract
• Rumora AE,Steere AN,Ramsey JE,Knapp AM,Ballif BA,Kelm RJ Jr. Isolation and characterization of the core single-stranded DNA-binding domain of purine-rich element binding protein B (Purβ) Biochemical and Biophysical Research Communications. 2010, 400:340-5. Abstract
• Lechtreck KF, Johnson EC, Sakai T, Cochran D, Ballif BA, Rush J, Pazour GJ, Ikebe M, Witman GB.The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella.Journal of Cell Biology. 2009, 187:1117-32. Abstract
• Miller MS, Lekkas P, Braddock JM, Farman GP, Ballif BA, Irving TC, Maughan DW, Vigoreaux JO. Aging enhances indirect flight muscle fiber performance yet decreases flight ability in Drosophila. Biophysical Journal. 2008, 95:2391-401. Abstract
• W.M. Brieher, H.Y. Kueh, B.A. Ballif, and T.J. Mitchison. Rapid, actin monomer insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. Journal of Cell Biology, 2006, 175:315-24. Abstract

 

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