Dr Mark Graham

Senior Lecturer, Medicine
Group Leader, Children's Medical Research Institute

Telephone +61 2 8865 2989

Website PhD at the Children's Medical Research Institute
Honours in Medical Sciences at Westmead

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Research interests

Dr Graham’s overall aim is to understand the molecular basis of neurological diseases. In particular, his group is focusing on proteins involved in neurotransmission, how they interact, mapping cellular signalling events triggered by neurotransmission and identifying regulatory mechanisms that could potentially be exploited by therapeutics for diseases of neurotransmission, e.g. epilepsy, autism, schizophrenia, bipolar disorder, etc.

The Synapse Proteomics Group uses cutting edge technology and basic biochemical and molecular biology techniques. In particular, Dr Graham studies protein phosphorylation to determine critical dynamic signalling events. Phosphoproteomics is being applied as a tool to screen for key proteins and pathways that mediate presynaptic plasticity. Screens are followed by biochemical analysis and functional assays to discover new mechanisms and their consequences for neurotransmitter release and neurological diseases.

The biogenesis of synaptic vesicles via endocytosis is important for neurotransmission and is also a focus. His group is determining the mechanisms of how vesicles are made by investigation of the protein complex that forms a clathrin coat over budding vesicles (a complex of clathrin, the adapter protein complex 2 and assembly protein AP180). This mechanism regulates quantal neurotransmitter release by controlling the size of synaptic vesicles.

Selected grants

2015

  • To investigate the role of ATM protein in protecting against neurodegeneration; Lavin M, Roberts T, Graham M; National Health and Medical Research Council (NHMRC)/Project Grants.
  • Phosphatase regulators mediate long-term changes in presynaptic terminals; Graham M, Robinson P; National Health and Medical Research Council (NHMRC)/Project Grants.

2014

  • Aberrant mesenchymal-epithelial transition: a pathogenic mechanism in tissue maintenance and differentiation; Tam P, Loebel D, Graham M, Arthur J; National Health and Medical Research Council (NHMRC)/Project Grants.

2013

  • Phosphorylation of synaptic vesicle glycoprotein 2 (SV2) regulates endocytosis of synaptotagmin for synaptic transmission; Robinson P, Graham M; National Health and Medical Research Council (NHMRC)/Project Grants.

2012

  • A Pilot Study of Pre-synaptic Protein Kinases; Graham M, Robinson P; DVC Research/Bridging Support Grant.
  • Role of oxidative stress in the human genetic disorder ataxia telangiectasia; Graham M, Lavin M; National Health and Medical Research Council (NHMRC)/Project Grants.

2011

  • Identification of the phospho-regulated synaptic vesicle endocytosis machinery; Graham M, Robinson P; Rebecca L Cooper Medical Research Foundation/Equipment Grant.

2009

  • Inhibitory signaling switches define the machinery of synaptic vesicle endocytosis; Graham M; National Health and Medical Research Council (NHMRC)/Career Development Awards.
  • Inhibitory signaling switches define the machinery of synaptic vesicle endocytosis; Graham M; DVC Research/Research Fellow Establishment Grants.
  • O-GlcNAc-phosphorylation: a novel post-translational modification regulating vesicle recycling.; Graham M, Robinson P; Australian Research Council (ARC)/Discovery Projects (DP).
  • Mechanisms of synaptic vesicle endocytosis revealed by its regulatory phosphoproteome; Robinson P, Graham M; National Health and Medical Research Council (NHMRC)/Project Grants.

Selected publications

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Journals

  • Kozlov, S., Waardenberg, A., Engholm-Keller, K., Arthur, J., Graham, M., Lavin, M. (2016). ROS-activated ATM-dependent phosphorylation of cytoplasmic substrates identified by large scale phosphoproteomics screen. Molecular and Cellular Proteomics, 15(3), 1032-1047. [More Information]
  • Yeo, A., Becherel, O., Luff, J., Graham, M., Richard, D., Lavin, M. (2015). Senataxin controls meiotic silencing through ATR activation and chromatin remodeling. Cell Discovery, 1, 1-20. [More Information]
  • Moshkanbaryans, L., Chan, L., Graham, M. (2014). The Biochemical Properties and Functions of CALM and AP180 in Clathrin Mediated Endocytosis. Membranes, 4(3), 388-413. [More Information]
  • Chan, L., Moshkanbaryans, L., Xue, J., Graham, M. (2014). The ~ 16 kDa C-terminal sequence of clathrin assembly protein AP180 is essential for efficient clathrin binding. PloS One, 9(10), 1-13. [More Information]
  • Parker, B., Thaysen-Andersen, M., Solis, N., Scott, N., Larsen, M., Graham, M., Packer, N., Cordwell, S. (2013). Site-Specific Glycan-Peptide Analysis for Determination of N-Glycoproteome Heterogeneity. Journal of Proteome Research, 12(12), 5791-8000. [More Information]
  • Palmisano, G., Parker, B., Engholm-Keller, K., Lendal, S., Kulej, K., Schulz, M., Schwammle, V., Graham, M., Saxtorph, H., Cordwell, S., et al (2012). A novel method for the simultaneous enrichment, identification, and quantification of phosphopeptides and sialylated glycopeptides applied to a temporal profile of mouse brain development. Molecular and Cellular Proteomics, 11(11), 1191-1202. [More Information]
  • Bolderson, E., Savage, K., Mahen, R., Pisupati, V., Graham, M., Richard, D., Robinson, P., Venkitaraman, A., Khanna, K. (2012). Kruppel-associated Box (KRAB)-associated co-repressor (KAP-1) Ser-473 phosphorylation regulates heterochromatin protein 1B (HP1-B) mobilization and DNA repair in heterochromatin. Journal of Biological Chemistry, 287(33), 28122-28131. [More Information]
  • Quan, A., Xue, J., Wielens, J., Smillie, K., Anggono, V., Parker, M., Cousin, M., Graham, M., Robinson, P. (2012). Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation. Proceedings of the National Academy of Sciences of the United States of America (PNAS), 109(10), 3760-3765. [More Information]
  • Graham, M., Thaysen-Andersen, M., Bache, N., Craft, G., Larsen, M., Packer, N., Robinson, P. (2011). A Novel Post-translational Modification in Nerve Terminals: O-Linked N-Acetylglucosamine Phosphorylation. Journal of Proteome Research, 10(6), 2725-2733. [More Information]
  • Kozlov, S., Graham, M., Jakob, B., Tobias, F., Kijas, A., Tanuji, M., Chen, P., Robinson, P., Taucher-Scholz, G., Suzuki, K., et al (2011). Autophosphorylation and ATM activation: additional sites add to the complexity. Journal of Biological Chemistry, 286(11), 9107-9119. [More Information]
  • Xue, J., Graham, M., Novelle, A., Sue, N., Gray, N., McNiven, M., Smillie, K., Cousin, M., Robinson, P. (2011). Calcineurin Selectively Docks with the Dynamin Ixb Splice Variant to Regulate Activity-dependent Bulk Endocytosis. Journal of Biological Chemistry, 286(35), 30295-30303. [More Information]
  • Chircop (nee Fabbro), M., Sarcevic, B., Larsen, M., Malladi, C., Chau, N., Zavortink, M., Smith, C., Quan, A., Anggono, V., Hains, P., Graham, M., Robinson, P. (2011). Phosphorylation of dynamin II at serine-764 is associated with cytokinesis. BBA: Biochimica et Biophysica Acta - Molecular Cell Research, 1813 (10), 1689-1699. [More Information]
  • Chan, L., Hansra, G., Robinson, P., Graham, M. (2010). Differential Phosphorylation of Dynamin I Isoforms in Subcellular Compartments Demonstrates the Hidden Complexity of Phosphoproteomes. Journal of Proteome Research, 9(8), 4028-4037. [More Information]
  • Baker, M., Smith, N., Hetherington, L., Taubman, K., Graham, M., Robinson, P., Aitken, R. (2010). Label-Free Quantitation of Phosphopeptide Changes During Rat Sperm Capacitation. Journal of Proteome Research, 9(2), 718-729. [More Information]
  • O'dell, L., Chau, N., Mariana, A., Graham, M., Robinson, P., McCluskey, A. (2009). Azido and Diazarinyl Analogues of Bis-Tyrphostin as Asymmetrical Inhibitors of Dynamin GTPase. ChemMedChem: chemistry enabling drug discovery, 4(7), 1182-1188. [More Information]
  • Chircop (nee Fabbro), M., Oakes, V., Graham, M., Ma, M., Smith, C., Robinson, P., Khanna, K. (2009). The actin-binding and bundling protein, EPLIN, is required for cytokinesis. Cell Cycle, 8(5), 757-764. [More Information]
  • Craft, G., Graham, M., Bache, N., Larsen, M., Robinson, P. (2008). The in vivo phosphorylation sites in multiple isoforms of amphiphysin I from rat brain nerve terminals. Molecular and Cellular Proteomics, 7(6), 1146-1161. [More Information]
  • Cohen, S., Graham, M., Lovrecz, G., Bache, N., Robinson, P., Reddel, R. (2007). Protein composition of catalytically active human telomerase from immortal cells. Science, 315(5820), 1850-1853. [More Information]
  • Oganesian, L., Graham, M., Robinson, P., Bryan, T. (2007). Telomerase Recognizes G-Quadruplex and Linear DNA as Distinct Substrates. Biochemistry, 46(40), 11279-11290. [More Information]
  • Graham, M., Kilby, D., Firth, S., Robinson, P., Baxter, R. (2007). The in vivo phosphorylation and glycosylation of human insulin-like growth factor binding protein-5. Molecular and Cellular Proteomics, 6(8), 1392-1405. [More Information]
  • Graham, M., Anggono, V., Bache, N., Larsen, M., Craft, G., Robinson, P. (2007). The in vivo phosphorylation sites of rat brain dynamin I. Journal of Biological Chemistry, 282(20), 14695-14707. [More Information]
  • Acevedo, K., Li, R., Soo, P., Suryadinata, R., Sarcevic, B., Valova, V., Graham, M., Robinson, P., Bernard, O. (2007). The phosphorylation of p25/TPPP by LIM kinase 1 inhibits its ability to assemble microtubules. Experimental Cell Research, 313(20), 4091-4106. [More Information]
  • Kozlov, S., Graham, M., Peng, C., Chen, P., Robinson, P., Lavin, M. (2006). Involvement of novel autophosphorylation sites in ATM activation. The EMBO Journal, 25(15), 3504-3514.
  • Anggono, V., Smillie, K., Graham, M., Valova, V., Cousin, M., Robinson, P. (2006). Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nature Neuroscience, 9(6), 752-760. [More Information]
  • Chircop (nee Fabbro), M., Zhou, B., Takahashi, M., Sarcevic, B., Lal, P., Graham, M., Gabrielli, B., Robinson, P., Nigg, E., Ono, Y., et al (2005). Cdk1/Erk2- and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Developmental Cell, 9(4), 477-488. [More Information]
  • Hill, T., O'dell, L., Edwards, J., Graham, M., McGeachie, A., Rusak, J., Quan, A., Abagyan, R., Scott, J., Robinson, P., et al (2005). Small molecule inhibitors of dynamin I GTPase activity: Development of dimeric tyrphostins. Journal of Medicinal Chemistry, 48(24), 7781-7788.
  • Larsen, M., Graham, M., Robinson, P., Roepstorff, P. (2004). Improved Detection Of Hydrophilic Phosphopeptides Using Graphite Powder Microcolumns And Mass Spectrometry: Evidence For In Vivo Doubly Phosphorylated Dynamin I And Dynamin Iii. Molecular and Cellular Proteomics, 3(5), 456-465.
  • Graham, M., Ruma-Haynes, P., Capes-Davis, A., Dunn, J., Tan, T., Valova, V., Robinson, P., Jeffrey, P. (2004). Multisite Phosphorylation Of Doublecortin By Cyclin-Dependent Kinase 5. Biochemical Journal, 381(2), 471-481.
  • Xue, J., Milburn, P., Hanna, B., Graham, M., Rostas, J., Robinson, P. (2004). Phosphorylation Of Septin 3 On Ser-91 By Cgmp-Dependent Protein Kinase-I In Nerve Terminals. Biochemical Journal, 381(3), 753-760.
  • Tan, T., Valova, V., Malladi, C., Graham, M., Berven, L., Jupp, O., Hansra, G., McClure, S., Sarcevic, B., Boadle, R., Robinson, P., et al (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nature Cell Biology, 5(8), 701-710.

2016

  • Kozlov, S., Waardenberg, A., Engholm-Keller, K., Arthur, J., Graham, M., Lavin, M. (2016). ROS-activated ATM-dependent phosphorylation of cytoplasmic substrates identified by large scale phosphoproteomics screen. Molecular and Cellular Proteomics, 15(3), 1032-1047. [More Information]

2015

  • Yeo, A., Becherel, O., Luff, J., Graham, M., Richard, D., Lavin, M. (2015). Senataxin controls meiotic silencing through ATR activation and chromatin remodeling. Cell Discovery, 1, 1-20. [More Information]

2014

  • Moshkanbaryans, L., Chan, L., Graham, M. (2014). The Biochemical Properties and Functions of CALM and AP180 in Clathrin Mediated Endocytosis. Membranes, 4(3), 388-413. [More Information]
  • Chan, L., Moshkanbaryans, L., Xue, J., Graham, M. (2014). The ~ 16 kDa C-terminal sequence of clathrin assembly protein AP180 is essential for efficient clathrin binding. PloS One, 9(10), 1-13. [More Information]

2013

  • Parker, B., Thaysen-Andersen, M., Solis, N., Scott, N., Larsen, M., Graham, M., Packer, N., Cordwell, S. (2013). Site-Specific Glycan-Peptide Analysis for Determination of N-Glycoproteome Heterogeneity. Journal of Proteome Research, 12(12), 5791-8000. [More Information]

2012

  • Palmisano, G., Parker, B., Engholm-Keller, K., Lendal, S., Kulej, K., Schulz, M., Schwammle, V., Graham, M., Saxtorph, H., Cordwell, S., et al (2012). A novel method for the simultaneous enrichment, identification, and quantification of phosphopeptides and sialylated glycopeptides applied to a temporal profile of mouse brain development. Molecular and Cellular Proteomics, 11(11), 1191-1202. [More Information]
  • Bolderson, E., Savage, K., Mahen, R., Pisupati, V., Graham, M., Richard, D., Robinson, P., Venkitaraman, A., Khanna, K. (2012). Kruppel-associated Box (KRAB)-associated co-repressor (KAP-1) Ser-473 phosphorylation regulates heterochromatin protein 1B (HP1-B) mobilization and DNA repair in heterochromatin. Journal of Biological Chemistry, 287(33), 28122-28131. [More Information]
  • Quan, A., Xue, J., Wielens, J., Smillie, K., Anggono, V., Parker, M., Cousin, M., Graham, M., Robinson, P. (2012). Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation. Proceedings of the National Academy of Sciences of the United States of America (PNAS), 109(10), 3760-3765. [More Information]

2011

  • Graham, M., Thaysen-Andersen, M., Bache, N., Craft, G., Larsen, M., Packer, N., Robinson, P. (2011). A Novel Post-translational Modification in Nerve Terminals: O-Linked N-Acetylglucosamine Phosphorylation. Journal of Proteome Research, 10(6), 2725-2733. [More Information]
  • Kozlov, S., Graham, M., Jakob, B., Tobias, F., Kijas, A., Tanuji, M., Chen, P., Robinson, P., Taucher-Scholz, G., Suzuki, K., et al (2011). Autophosphorylation and ATM activation: additional sites add to the complexity. Journal of Biological Chemistry, 286(11), 9107-9119. [More Information]
  • Xue, J., Graham, M., Novelle, A., Sue, N., Gray, N., McNiven, M., Smillie, K., Cousin, M., Robinson, P. (2011). Calcineurin Selectively Docks with the Dynamin Ixb Splice Variant to Regulate Activity-dependent Bulk Endocytosis. Journal of Biological Chemistry, 286(35), 30295-30303. [More Information]
  • Chircop (nee Fabbro), M., Sarcevic, B., Larsen, M., Malladi, C., Chau, N., Zavortink, M., Smith, C., Quan, A., Anggono, V., Hains, P., Graham, M., Robinson, P. (2011). Phosphorylation of dynamin II at serine-764 is associated with cytokinesis. BBA: Biochimica et Biophysica Acta - Molecular Cell Research, 1813 (10), 1689-1699. [More Information]

2010

  • Chan, L., Hansra, G., Robinson, P., Graham, M. (2010). Differential Phosphorylation of Dynamin I Isoforms in Subcellular Compartments Demonstrates the Hidden Complexity of Phosphoproteomes. Journal of Proteome Research, 9(8), 4028-4037. [More Information]
  • Baker, M., Smith, N., Hetherington, L., Taubman, K., Graham, M., Robinson, P., Aitken, R. (2010). Label-Free Quantitation of Phosphopeptide Changes During Rat Sperm Capacitation. Journal of Proteome Research, 9(2), 718-729. [More Information]

2009

  • O'dell, L., Chau, N., Mariana, A., Graham, M., Robinson, P., McCluskey, A. (2009). Azido and Diazarinyl Analogues of Bis-Tyrphostin as Asymmetrical Inhibitors of Dynamin GTPase. ChemMedChem: chemistry enabling drug discovery, 4(7), 1182-1188. [More Information]
  • Chircop (nee Fabbro), M., Oakes, V., Graham, M., Ma, M., Smith, C., Robinson, P., Khanna, K. (2009). The actin-binding and bundling protein, EPLIN, is required for cytokinesis. Cell Cycle, 8(5), 757-764. [More Information]

2008

  • Craft, G., Graham, M., Bache, N., Larsen, M., Robinson, P. (2008). The in vivo phosphorylation sites in multiple isoforms of amphiphysin I from rat brain nerve terminals. Molecular and Cellular Proteomics, 7(6), 1146-1161. [More Information]

2007

  • Cohen, S., Graham, M., Lovrecz, G., Bache, N., Robinson, P., Reddel, R. (2007). Protein composition of catalytically active human telomerase from immortal cells. Science, 315(5820), 1850-1853. [More Information]
  • Oganesian, L., Graham, M., Robinson, P., Bryan, T. (2007). Telomerase Recognizes G-Quadruplex and Linear DNA as Distinct Substrates. Biochemistry, 46(40), 11279-11290. [More Information]
  • Graham, M., Kilby, D., Firth, S., Robinson, P., Baxter, R. (2007). The in vivo phosphorylation and glycosylation of human insulin-like growth factor binding protein-5. Molecular and Cellular Proteomics, 6(8), 1392-1405. [More Information]
  • Graham, M., Anggono, V., Bache, N., Larsen, M., Craft, G., Robinson, P. (2007). The in vivo phosphorylation sites of rat brain dynamin I. Journal of Biological Chemistry, 282(20), 14695-14707. [More Information]
  • Acevedo, K., Li, R., Soo, P., Suryadinata, R., Sarcevic, B., Valova, V., Graham, M., Robinson, P., Bernard, O. (2007). The phosphorylation of p25/TPPP by LIM kinase 1 inhibits its ability to assemble microtubules. Experimental Cell Research, 313(20), 4091-4106. [More Information]

2006

  • Kozlov, S., Graham, M., Peng, C., Chen, P., Robinson, P., Lavin, M. (2006). Involvement of novel autophosphorylation sites in ATM activation. The EMBO Journal, 25(15), 3504-3514.
  • Anggono, V., Smillie, K., Graham, M., Valova, V., Cousin, M., Robinson, P. (2006). Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nature Neuroscience, 9(6), 752-760. [More Information]

2005

  • Chircop (nee Fabbro), M., Zhou, B., Takahashi, M., Sarcevic, B., Lal, P., Graham, M., Gabrielli, B., Robinson, P., Nigg, E., Ono, Y., et al (2005). Cdk1/Erk2- and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Developmental Cell, 9(4), 477-488. [More Information]
  • Hill, T., O'dell, L., Edwards, J., Graham, M., McGeachie, A., Rusak, J., Quan, A., Abagyan, R., Scott, J., Robinson, P., et al (2005). Small molecule inhibitors of dynamin I GTPase activity: Development of dimeric tyrphostins. Journal of Medicinal Chemistry, 48(24), 7781-7788.

2004

  • Larsen, M., Graham, M., Robinson, P., Roepstorff, P. (2004). Improved Detection Of Hydrophilic Phosphopeptides Using Graphite Powder Microcolumns And Mass Spectrometry: Evidence For In Vivo Doubly Phosphorylated Dynamin I And Dynamin Iii. Molecular and Cellular Proteomics, 3(5), 456-465.
  • Graham, M., Ruma-Haynes, P., Capes-Davis, A., Dunn, J., Tan, T., Valova, V., Robinson, P., Jeffrey, P. (2004). Multisite Phosphorylation Of Doublecortin By Cyclin-Dependent Kinase 5. Biochemical Journal, 381(2), 471-481.
  • Xue, J., Milburn, P., Hanna, B., Graham, M., Rostas, J., Robinson, P. (2004). Phosphorylation Of Septin 3 On Ser-91 By Cgmp-Dependent Protein Kinase-I In Nerve Terminals. Biochemical Journal, 381(3), 753-760.

2003

  • Tan, T., Valova, V., Malladi, C., Graham, M., Berven, L., Jupp, O., Hansra, G., McClure, S., Sarcevic, B., Boadle, R., Robinson, P., et al (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nature Cell Biology, 5(8), 701-710.

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