Macrophages play an important role in host defense against invading micro-organisms and they are also key players in initiating and maintaining an immune response. However, macrophages can also play negative roles, such as in chronic inflammatory diseases. Also, tumor-associated macrophages (TAMs), which are present in large numbers in many tumors, appear to play an important role in promoting the progression of solid tumors to an invasive, metastatic phenotype. Macrophages are therefore a prime target for therapies, but it is important to elucidate the mechanisms by which they are recruited to and activated in tissues.

1.    Abou-Kheir, W.G., Isaac, B., Yamaguchi H., and Cox, D. (2008) Membrane targeting of WAVE2 is not sufficient for WAVE2 dependent actin polymerization: a role for IRSp53 in mediating the interaction between Rac and WAVE2. J. Cell Sci. 121:379-90. PMCID:PMC2749557

2.    Hernandez-Tellez, Smirnova, T., Kedrin, D., L., Wyckoff, J., Stanley, E.R., Cox, D., Muller, W.J., Pollard, J.W., Van Rooijen, N., and J. Segall. (2009) EGF/CSF1Induced Breast Cancer Cell Invasion is Triggered by Heregulin Beta 1 and CXCL12. Cancer Research 69:3221-3227. PMCID:PMC2820720

3.    Ojalvo, L.S., King, W., Cox, D., and J.W. Pollard (2009) High Density Gene Expression Analysis of Tumor Associated Macrophages from Mouse Mammary Tumors. Amer. J. Path. 174:1048-1064. PMCID:PMC2665764

4.    Cammer, M., Gevrey, J-C., Lorenz, M., Dovas, A., Condeelis, J. and Cox, D. (2009) The mechanism of CSF-1 induced WASp activation in vivo: A role of PI 3-kinase and Cdc42. J. Biol. Chem. 284:23302-11. PMCID:PMC2749104

5.    Luo, Y., Isaac, B.M., Casadevall, A., and Cox D. (2009) Macrophage phagocytosis suppresses F-actin enriched membrane protrusions stimulated by CX3CL1 and CSF-1. Infect. and Immun. 77:4487-4495. PMCID:PMC2747920

6.    Park, H. and Cox, D. (2009) Cdc42 regulated Fcγ receptor mediated phagocytosis through activation and phosphorylation of WASP and N-WASP. Molec. Biol. Cell 20:4500-8. PMCID:PMC2770938

7.    Dovas, A., Gevrey, J-C., Grossi, A., Park, H., Abou-Kheir, W.A., and Cox, D. (2009) Regulation of podosome dynamics by Wiskott-Aldrich Syndrome protein (WASp) phosphorylation: implication in matrix degradation and chemotaxis in macrophages. J. Cell Sci. 122:3873-82. PMCID:PMC2773189

8.    Isaac, B.M.*, Ishihara, D.*, Nusblat, L.M., Gevrey, J-C, Dovas A., Condeelis, J., and Cox, D. (2010) N-WASP has the Ability to Compensate for the Loss of WASP in Macrophage Podosome Formation and Function. Exp. Cell Res. 316:3406-3416. PMCID: PMC2976787 * equal contribution.

9.Nusblat, L.M., Dovas, A., and Cox. D. (2011). The non-redundant role of N-WASP in podosome-mediated matrix degradation in macrophages. Eur. J. Cell Biol. 90:205-212. PMCID: PMC3012153

10. Oser, M., Dovas, A., Cox, D., and Condeelis, J. (2011) Nck1 and Grb2 localization patterns can distinguish invadopodia from podosomes. Eur. J. Cell Biol. 90:181-188. PMCID: PMC3017226

11. Park, H. and Cox, D. (2011) Syk regulates multiple signaling pathways leading to CX3CL1 chemotaxis in macrophages. J. Biol. Chem. 286:14762-9. PMCID: PMC3083178

12. Dovas, A., Gligorijevic, B., Chen, X., Entenberg, D., Condeelis, J. and Cox, D. (2011) Visualisation of actin dynamics in invasive structures of macrophages and carcinoma cells using photoconvertible b-actin – Dendra2 fusion proteins. PLoS One 6:e16485. PMCID: PMC3038862

13.    Dovas, A. and Cox, D. (2011) Signaling networks regulating leukocyte podosome dynamics and function. Cell Signal.23:1225-34. PMCID: PMC3095719

14. Sampaio, N., Yu, W., Cox, D., Wyckoff, J., Condeelis, J., Stanley, E.R., and Pixley, F.J. (2011). Phosphorylation of Y721 of the CSF-1R mediates PI3K association to regulate macrophage motility and enhancement of tumor cell invasion. J. Cell Sci. 124:2021-31. PMCID: PMC3104034

15. Park, H., Dovas, A. and Cox, D. (2011) N-WASP. In Encyclopedia of Signaling Molecules. Ed. by S. Choi (Springer).

16. Mahankali, M., Peng, H-J, Cox, D., and Gomez-Cambronero, J. (2011) The Mechanism of Cell Membrane Protrusion Formation Relies on a Phospholipase D2, GRB2 AND Rac2 Association. Cell Signal. 23:1291-8. PMCID: PMC3095729

17. Kantonen, S., Mahankali, M., Hatton, N., Park, H., Cox, D., and Gomez-Cambronero J. (2011) A two-step mechanism of leukocyte phagocytosis involves the formation of a novel PLD-Grb2-WASp protein heterotrimer. Molec. Cell Biol. 31:4524-37 PMCID: PMC3209255

18. Ishihara, D., Dovas A., Park, H., Isaac, B.M., and Cox, D. (2012) The Chemotactic defect in Wiskott-Aldrich Syndrome macrophages is due to reduced persistence of directional protrusions. PLoS One 7(1):e30033 PMCID:PMC3261183 

19. Boimel P., Smirnova T., Zhou, Z., Wyckoff J., Park H., Coniglio, S., Patel P., Qian, B., Stanley, E.R., Bresnick A., Cox D.,  Pollard J.W., Muller W.J., Condeelis J, Segall J.E. (2012) Contribution of CXCL12 secretion to invasion of breast cancer cells. Cancer Res. 14:R23 PMCID: PMC3496141

20. Ishihara, D., Dovas A., Isaac, B.M., and Cox, D. (2012) The Chemotactic defect in Wiskott-Aldrich Syndrome macrophages is due to reduced persistence of directional protrusions. PLoS One 7(1):e30033 PMCID:PMC3261183.

21. Sharma, V., Patsialou, A., Beaty, B.T.,  Liu, H., Clarke, M., Cox, D., Condeelis, J. and Eddy, R. (2012) Reconstitution of in vivo macrophage-tumor cell pairing and streaming motility on one-dimensional micro-patterned substrates. IntraVital 1:77-85.

18. Dovas. A., Patsialou, A., Harney, A.S., Condeelis, J. and Cox, D. (2012) Imaging interactions between macrophages and tumor cells that are involved in metastasis in vivo.J. Microscopy doi: 10.1111/j.1365-2818.2012.03667 PMID:PMC23198984

19. Ishihara, D.*, Dovas, A.*, Hernandez, L., Pozzuto, M., Wyckoff, J., Segall, J., Condeelis, J., Bresnick, B., and Cox, D. (2013) Wiskott-Aldrich syndrome protein regulates leukocyte-dependent breast cancer metastasis. Cell Reports 4:429-436    PMCID: PMC3777703

20. Rougerie, P., Miskolci, V. and Cox, D. (2013) Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton. Immunol. Reviews. 256:222-239. PMCID:PMC3806206

21. Park, H., Dovas, A., Hanna, S., Cougoule, C, Marridoneau-Parini, I., and Cox, D. (2014) Tyrosine phosphorylation of Wiskott-Aldrich Syndrome protein (WASP) by Hck regulates Macrophage Function. J. Biol. Chem. 289(11):7897-906 PMCID: 24482227.

22. Hanna, S., Miskolci, V., Cox, D.* and Hodgson, L.* (2014) Development of a new single-chain genetically encoded Cdc42 FRET biosensor. PLoS One 9(5):e96469 PMCID:24798463. *co-corresponding authors

23. Miskolci, V., Spiering, D., Cox, D., and Hodgson, L. (2014) A mix-and-measure assay for determining the activation status of endogenous Cdc42 in cell lysates. Methods in Molecular Biology: Cytokines. 1172:173-84. PMID:24908304

24. Sharma, V. P., Beaty, B.T., Cox, D., Condeelis, J.S., and Eddy, R.J. (2014) An in vitro one-dimensional assay to study growth factor-regulated tumor cell-macrophage interaction. Methods in Molecular Biology: Cytokines. 1172:173-84. PMID:24908304

25. Cammer, M., and Cox, D. (2014) Chemotactic Responses by Macrophages to a Directional Source of a Cytokine Delivered by a Micropipette. Methods in Molecular Biology: Cytokines. 1172:125-35. PMID:24908300

26. Hind, L., Cox, D., and Hammer, D., (2014) Microcontact Printing of Fibronectin Elicits Motility in a Macrophage Cell Line. Cytoskeleton doi: 10.1002/cm.21191. PMID:2518681

27.    Pignatelli, J., Goswami, S, Jones, J.G., Rohan, T.E., Pieri, E., Chen, X., Adler, E., Maleki, S., Cox, D., Bresnick, A., Gertler, F.B., Condeelis, J.S.,  and Oktay, M.H. (2014) Invasive Breast Carcinoma Cells from Patients Exhibit MenaINV- and Macrophage-Dependent Transendothelial Migration. Science Signaling 7(353):ra112/scisignal.2005329. PMCID: PMC426693

28.   Wu, B.*, Miskolci, V.*, Donnelly, S.K., Cox, D., Singer, R.H.^% and Hodgson L.^% (2015) Synonymous modification of repeated sequences in retroviral reporters.  Genes Dev. 29 (8):876-86. PMCID:PMC4403262

29.    McCoy-Simandle, K., Hanna, S., and Cox, D. (2015) Exosomes and nanotubes: control of immune cell communication. Internat. J. Biochem. Cell Biol. 71:44-54. PMCID: PMC4720554

30.    Miskolci, V., Wu, B., Moshfegh, Y., Cox, D.*, and Hodgson L.* (2016) Optical tools to study the isoform-specific roles of small GTPases in immune cells. J. Immunol. 96:3479-93. PMCID:PMC4821714 *co-corresponding authors

31.    Janssen, E. *, Hedayat, M.*, Leick, M.*, Tohme, M.*, Kumari, S., Ramesh, N., Massad, M., Ullas, S., Azcutia Criado, V., Goodnow, C.G., Randall, K.L., Qaio, Q., Wu, H., Cox, D., Hartwig, J., Irvine, D.J., Luscinskas, F.W., and Geha, R.S. (2016) A DOCK8-WIP-WASP complex links the TCR to the actin cytoskeleton. J. Clin. Invest. 126(10):3837-3851. PMID:27599296

32.    Leung, E., Xue, A., Wang, Y., Rougerie, P., Sharma, V., Eddy, R., Cox, D., and J. Condeelis (2017) Blood vessel endothelium -directed tumor cell streaming in breast tumors requires the HGF/C-Met signaling pathway. Oncogene 36(19):2680-2692. PMID:PMC5426963

33.    Miskolci, V., Hodgson, L., Cox, D. (2017) Using FRET-based biosensors to probe Rho GTPase activation during phagocytosis. Methods in Molecular Biology: Phagocytosis and Phagosome Maturation. 1519:125-143. PMCID: PMC5116239

34.    Hanna, S.*, McCoy-Simandle, K.*, Miskolci, V., Guo, P., Cammer, M., Hodgson, L., and Cox, D. (2017) The Role of Rho-GTPases and actin polymerization during Macrophage Tunneling Nanotube Biogenesis. Sci. Reports 17;7(1):8547. doi: 10.1038/s41598-017-08950-7. PMCID:PMC5561213  *co-first authors

35.    Donnelly, S.K.*, Miskolci, V.*, Garrastegui, A.M., Cox, D., and Hodgson, L. (2018) Characterization of genetically encoded FRET biosensors for Rho family GTPases. Methods in Molecular Biology: Rho GTPases. Methods Mol Biol. 2018;1821:87-106. PMID:30062407  *co-first authors

36.      Hanna, S.J., McCoy-Simandle, K., Genna, A., Leung, E., Condeelis, J., Cox, D. (2019) Tunneling Nanotubes, a Novel Mode of Tumor Cell-Macrophage Communication in Tumor Cell Invasion. J. Cell Science. 132(3). pii: jcs223321. doi: 10.1242/jcs.223321. PMID:30659112.

37.      Carter, K.P., Hanna, S., Genna, A., Lewis, D., Segall., Cox, D. (2019) Macrophage induced tumor cell tunneling nanotubes enhance tumor cell 3D invasion. Cancer reports 2(9).

38.    Mighty, J., Sauma, S., Hanna, S., Muntzel, M., Molina, H., Cox, D., Redenti, S. (2020) Analysis of adult neural retina extracellular vesicle release, cell to cell RNA transport and proteomic cargo. Investigative Ophthalmology & Visual Science. Feb 7;61(2):30. doi: 10.1167/iovs.61.2.30.

39.      Carter, K.P., Segall, J.E., Cox, D. (2020) Microscopic Methods for Analysis of Macrophage Induced Tunneling Nanotubes. Methods in Molecular Biology: Immune Mediators in Cancer. 2108:273-279. doi: 10.1007/978-1-0716-0247-8_23. PMID: 31939188

40.    Al Haddad M, El-Rif R, Hanna S, Jaafar L, Dennaoui R, Abdellatef S, Miskolci V, Cox D, Hodgson L, El-Sibai M. (2020) Differential regulation of rho GTPases during lung adenocarcinoma migration and invasion reveals a novel role of the tumor suppressor StarD13 in invadopodia regulation. Cell Commun Signal 8(1):144. doi: 10.1186/s12964-020-00635-5. PMCID: PMC7487901

41.   Genna, A., Duran, C., Entenberg, D., Condeelis, J., and Cox, D. (2023) Macrophages Promote Tumor cell Extravasation across an Endothelial Barrier through Thin Membranous Connections. Cancers, special issue “The Role of Tunneling Nanotubes in Intercellular Communication and Pathophysiology of Cancer” 15(7):2092. doi: 10.3390/cancers15072092