Publications

Johanna Joyce Lab publications

Selected Publications

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Click on the links below or see all Joyce lab and collaborative publications on Europe PMC.

Watson SS, Duc B, Kang Z, de Tonnac A, Eling N, Font L, Whitmarsh T, Massara M, IMAXT Consortium, Bodenmiller B, Hausser J, and Joyce JA (2024). Microenvironmental reorganisation in brain tumors following radiotherapy and recurrence revealed by hyperplexed immunofluorescence imaging (HIFI). Nature Communications, 15(1):3226, doi: 10.1038/s41467-024-47185-9.

Joyce JA (2024). How I made my lab meetings more inclusive with a rapid-relay technique. Commissioned ‘Careers feature’ for Nature.

Joyce JA (2024). Trans-Atlantic twists and turns. Invited perspective for Nature Cancer 5: 693-694.

Joyce JA, Masina S, Michalik L, Pot C, Sempoux C, Amati F (2024). Closing the scissor-shaped curve: strategies to promote gender equality in academia. Cell 187: 1335-1342.

Bejarano L, Kauzlaric A, Lamprou E, Lourenco J, Fournier N, Ballabio M, Colotti R, Maas RR, Massara M, Soukup K, Lilja J, Brouland J-P, Hottinger AF, Daniel RT, Hegi ME, and Joyce JA (2024). Interrogation of endothelial and mural cells in brain metastasis reveals key immune-regulatory mechanisms. Cancer Cell 42: 378-395.

Massara M, Dolfi B, Wischnewski V, Nolan E, Held W, Malanchi I, and Joyce JA (2024). Investigation of a fluorescent reporter microenvironment niche labeling strategy in experimental brain metastasis. iScience 27: 110284.

Maas RR, Soukup K, Fournier N, Massara M, Galland S, Kornete M, Wischnewski V, Lourenco J, Croci D, Álvarez-Prado AF, Marie DN, Lilja J, Marcone R, Fernandez Calvo G, Santalla Mendez R, Aubel P, Bejarano L, Wirapati P, Ballasteros I, Hidalgo A, Hottinger AF, Brouland J-P, Daniel RT, Hegi ME, and Joyce JA (2023). The local microenvironment drives activation of neutrophils in human brain tumors. Cell 186: 4546-4566.

Wischnewski V, Maas RR, Aruffo PG, Soukup K, Galletti G, Kornete M, Galland S, Fournier N, Lilja J, Wirapati P, Lourenco J, Scarpa A, Daniel RT, Hottinger AF, Brouland J-P, Losurdo A, Voulaz E, Alloiso M, Hegi ME, Lugli E, and Joyce JA (2023). Phenotypic diversity of T cells in primary and metastatic brain tumors revealed by multiomic interrogation. Nature Cancer 4: 908–924.

Theis FJ, Dar D, Vento-Tormo R, Vicković S, Wang L, Kagohara LT, Rendeiro AF, and Joyce JA (2023). What do you most hope spatial molecular profiling will help us understand? Cell Systems 14: 423-427.

de Visser K and Joyce JA (2023). The evolving tumor microenvironment: from cancer initiation to metastatic outgrowth. Cancer Cell 41: 374-403.

Qian BZ and Joyce JA (2023). Obituary for Jeffrey W. Pollard (1950–2023). Immunity 56: 1153-1154.

Loi S, Settleman J, Joyce JA, Pramesh CS, Bernards R, Fan J, Merchant JL, Moslehi J, Sellers WR (2023). The next big questions in cancer research. Cell 186:1523-1527.

Croci D*, Zomer A*, Kowal J, and Joyce JA (2023). Cranial imaging window implantation technique for longitudinal multimodal imaging of the brain environment in live mice. STAR Protocols 4: 102197.

Álvarez-Prado ÁF, Maas RR, Soukup K, Klemm F, Kornete M, Krebs FS, Zoete V, Berezowska S, Brouland J-P, Hottinger AF, Daniel RT, Hegi ME, Joyce JA (2023). Immunogenomic analysis of human brain metastases reveals diverse immune landscapes across genetically distinct tumors. Cell Reports Medicine 4:100900, doi: 10.1016/j.xcrm.2022.100900

Croci D, Santalla Mendez R, Temme S, Soukup K, Fournier N, Zomer A, Colotti R, Wischnewski V, Flögel U, van Heeswijk R, and Joyce JA (2022). Longitudinal and non-invasive monitoring of the spatial and temporal dynamics of glioma-associated macrophages. Science Translational Medicine 14: eabo2952, doi: 10.1126/scitranslmed.abo2952

Chryplewicz A, Scotton J, Tichet M, Zomer A, Shchors K, Joyce JA, Homicsko K, and Hanahan D (2022). Immunogenic autophagy, reprogrammed macrophages, and remodeled vasculature in glioblastoma triggers tumor immunity. Cancer Cell 40:1111-1127.

Zomer A*, Croci D*, Kowal J, van Gurp L, and Joyce JA (2022). Multimodal imaging of the dynamic brain tumor microenvironment during glioblastoma progression and in response to treatment. iScience 25: 104570.

Bejarano L*, Jordao MC* and Joyce JA (2021). Therapeutic targeting of the tumor microenvironment. Cancer Discovery 11: 933-959.

Maas RR*, Soukup K*, Klemm F*, Kornete M, Bowman RL, Bedel R, Marie DN, Alvarez-Prado AF, Labes D, Wilson A, Brouland JP, Daniel RT, Hegi ME, and Joyce JA (2021). An integrated pipeline for the comprehensive analysis of immune cells in human brain tumour clinical samples. Nature Protocols 16: 4692-4721.

Klemm F, Möckl A, Salamero-Boix A, Alekseeva T, Schäffer A, Schulz M, Niesel K, Maas RR, Groth M, Elie BT, Bowman RL, Hegi ME, Daniel RT, Zeiner PS, Zinke J, Harter PN, Plate KH, Joyce JA# and Sevenich L# (2021). Compensatory CSF2-driven macrophage activation promotes adaptive resistance to CSF1R Inhibition in breast-to-brain metastasis. (# Joint corresponding authors). Nature Cancer 2: 1086-1101

Klemm F, Maas RR, Bowman RL, Kornete M, Soukup K, Nassiri S, Brouland JP, Iacobuzio-Donahue CA, Brennan C, Tabar V, Gutin PH, Daniel RT, Hegi ME, and Joyce JA (2020). Interrogation of the microenvironmental landscape in brain tumors reveals disease-specific alterations of immune cells. Cell 181(7):1643-1660.

Akkari L#, Bowman RL, Tessier J, Klemm F, Handgraaf S, de Groot M, Quail DF, Tillard L, Gadiot J, Huse JT, Brandsma D, Westerga J, Watts C, and Joyce JA# (2020). Dynamic changes in glioma macrophage populations after radiotherapy reveals CSF-1R inhibition as a strategy to overcome resistance. (# Corresponding authors). Science Translational Medicine 12(552):eaaw7843, doi: 10.1126/scitranslmed.aaw7843.

Valiente M, Van Swearingen AED, Anders CK, Bairoch A, Boire A, Bos PD, Cittelly DM, Erez N, Ferraro GB, Fukumura D, Gril B, Herlyn M, Holmen SL, Jain RK, Joyce JA, Lorger M, Massague J, Neman J, Sibson NR, Steeg PS, Thorsen F, Young LS, Varešlija D, Vultur A, Weis-Garcia F, and Winkler F (2020). Brain metastasis cell lines panel: a public resource of organotropic cell lines. Cancer Research 80: 4314-4323.

Bernards R, Jaffee E, Joyce JA, Lowe SW, Mardis ER, Morrison SJ, Polyak K, Sears CL, Vousden KH, Zhang Z (2020). A roadmap for the next decade in cancer research. Nature Cancer 1: 12-17.

Kowal J, Kornete M, and Joyce JA (2019). Re-education of macrophages as a therapeutic strategy in cancer. Immunotherapy 11: 677-689.

Aldape K, Brindle KM, Chesler L, Chopra R, Hajjar A, Gilbert MR, Gottardo N, Gutmann DH, Hargrave D, Holland EC, Jones DTW, Joyce JA, Kearns P, Kieran MW, Mellinghoff IK, Merchant M, Pfister SM, Pollard SM, Ramaswamy V, Rich JN, Robinson GW, Rowitch DH, Sampson JH, Taylor MD, Workman P, and Gilbertson RJ (2019). Challenges to curing primary brain tumors. Nature Reviews Clinical Oncology 16: 509-520.

Soukup K and Joyce JA (2018). A long-distance relay-tionship between tumor and bone. Immunity 48: 13-16.

Olson OC, Quail DF, and Joyce JA (2017). Obesity and the tumor microenvironment. Science 358: 1130-31.

Quail DF*, Olson OC*, Bhardwaj P, Walsh LA, Akkari L, Quick ML, Chen IC, Wendel N, Ben-Chetrit N, Walker J, Holt PR, Dannenberg AJ, and Joyce JA (2017). Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF. Nature Cell Biology 19:974-987.

Yan D, Kowal J, Akkari L, Schuhmacher AJ, Huse JT, West BL, and Joyce JA (2017). Inhibition of colony stimulating factor-1 receptor abrogates microenvironment-mediated therapeutic resistance in gliomas. Oncogene 36: 6049-6058.

Olson OC, Kim H, Quail DF, Foley EA, and Joyce JA (2017). Tumor-associated macrophages suppress the cytotoxic activity of antimitotic agents. Cell Reports 19:101-113.

Quail DF and Joyce JA (2017). The microenvironmental landscape of brain tumors. Cancer Cell 31:326-341

Quail DF and Joyce JA (2017). Molecular pathways: dissecting mechanisms of resistance to macrophage-targeted therapies. Clinical Cancer Research 23: 876-884.

Bowman RL, Klemm F, Akkari L, Pyonteck SM, Sevenich L, Quail DF, Dhara S, Simpson K, Gardner EE, Iacobuzio-Donahue C, Brennan CW, Tabar V, Gutin PH, and Joyce JA (2016). Macrophage ontogeny underlies differences in tumor-specific education in brain malignancies. Cell Reports 17: 2445-2459.

Yan D*, Wang H*, Bowman RL*, and Joyce JA (2016). STAT3 and STAT6 signaling pathways synergize to promote cathepsin secretion from macrophages via IRE1α activation. Cell Reports 16: 2914–2927.

Prudova A*, Gocheva V*, Auf dem Keller U*, Eckhard U*, Olson OC, Akkari L, Butler GS, Fortelny N, Lange PF, Mark JC, Joyce JA# and Overall CM# (2016). TAILS N-terminomics and proteomics show protein degradation dominates over proteolytic processing by cathepsins in pancreatic tumors. (# Joint senior authors). Cell Reports 16: 1762-1773.

Quail DF, Bowman RL, Akkari L, Quick ML, Schuhmacher AJ, Huse JT, Holland EC, Sutton JC, and Joyce JA (2016). The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science 352: 6288

Akkari L and Joyce JA (2016). Microenvironmental InterFereNce of metabolism regulates chemosensitivity. Cell Research 26: 867-8.

Akkari L*, Gocheva V*, Quick ML, Kester JC, Spencer AK, Garfall AL, Bowman RL, and Joyce JA (2016). Combined deletion of cathepsin protease family members reveals compensatory mechanisms in cancer. Genes and Development 30: 220-32.

Olson OC and Joyce JA (2015). Cysteine cathepsin proteases: regulators of cancer progression and therapeutic response. Nature Reviews Cancer 15: 712-29.

Joyce JA and Fearon DF (2015). T cell exclusion, immune privilege and the tumor microenvironment. Science 348: 74-80.

Klemm F and Joyce JA (2015). Microenvironmental regulation of therapeutic resistance in cancer. Trends in Cell Biology 25: 198-213.

Akkari L, Gocheva V, Kester JC, Hunter KE, Quick ML, Sevenich L, Wang HW, Peters C, Tang LH, Klimstra DS, Reinheckel T and Joyce JA (2014). Distinct functions of macrophage-derived and cancer cell-derived cathepsin Z combine to promote tumor malignancy via interactions with the extracellular matrix. Genes and Development 28: 2134-50.

Sevenich L and Joyce JA (2014). Pericellular proteolysis in cancer. Genes and Development 28: 2331-2347.

Sevenich L, Bowman R*, Mason SD*, Quail DF, Rapaport F, Elie BT, Brogi E, Brastianos P, Hahn WC, Holsinger L, Massague J, Leslie CS, and Joyce JA (2014). Analysis of tumour and stroma-supplied proteolytic networks reveals a brain metastasis-promoting role for cathepsin S. Nature Cell Biology 16: 876-88.

Bowman RL and Joyce JA (2014). Tumor-associated macrophages and microglia as therapeutic targets in glioblastoma. Immunotherapy 6: 663-666.

Alonso-Curbelo D, Riveiro-Falkenback E, Perez-Guijarro E, Cifdaloz M, Osterloh L, Olmeda D, Megias D, Canon E, Karras P, Calvo TG, Gomez-Lopez G, Grana O, Checinska A, Wang HW, Pisano DG, Pastor J, Ortiz-Romero P, Torro D, Hoek K, Rodriguez-Peralto JL, Joyce JA and Soengas MS (2014). RAB7 controls melanoma progression by exploiting a lineage-specific wiring of the endolysosomal pathway. Cancer Cell 26: 61-76.

Hunter KE, Palermo C, Kester JC, Simpson K, Li JP, Tang LH, Klimstra DS, Vlodavsky I, and Joyce JA (2014). Heparanase promotes lymphangiogenesis and tumor invasion in pancreatic neuroendocrine tumors. Oncogene 33: 1799-1808.

Pyonteck SM*, Akkari L*, Schuhmacher AJ*, Bowman RL, Sevenich L, Quail D, Olson OC, Quick M, Huse J, Teijeiro V, Setty M, Leslie C, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D, and Joyce JA (2013). CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nature Medicine 19: 1264-72.

Quail D and Joyce JA (2013). Microenvironmental regulation of tumor progression and metastasis. Nature Medicine 19: 1423-37.

Carmona-Fontaine C, Bucci V, Akkari L, Deforet M, Joyce JA and Xavier JB (2013). Emergence of spatial structure in the tumor microenvironment due to the Warburg effect. PNAS 110: 19402-19407.

Krajcovic M, Krishna S, Akkari L, Joyce JA and Overholtzer M (2013). mTor regulates phagosome and entotic vacuole fission. Mol Biol Cell 24: 3736-3745.

Hunter KE, Quick ML, Sadanandam A, Hanahan D, and Joyce JA (2013). Identification and characterization of poorly differentiated invasive carcinomas in a mouse model of pancreatic neuroendocrine tumorigenesis. PLoS ONE. 8(5): e64472.

Lujambio A, Akkari L, Simon L, Grace D, Tschaharganeh DF, Bolden JE, Zhao Z, Thapar V, Joyce JA, Krizhanovsky V, Lowe SW (2013). Non-cell-autonomous tumor suppression by p53. Cell 153: 449-60.

Olson OC and Joyce JA (2013). A splicing twist on metastasis. Science Translational Medicine 5(169): 169fs2.

Ryder M, Gild M, Hohl TM, Pamer E, Knauf J, Ghossein R, Joyce JA, Fagin JA (2013). Genetic and pharmacological targeting of CSF-1/CSF-1R inhibits tumor-associated macrophages and impairs BRAF-induced thyroid cancer progression. PLoS ONE. 2013;8(1): e54302.

Olson OC and Joyce JA (2013). Microenvironment-mediated resistance to anticancer therapies. Cell Research 23: 179-81.

Pyonteck SM, Gadea BB, Wang HW, Gocheva V, Hunter KE, Tang LH and Joyce JA (2012). Deficiency of the macrophage growth factor Csf-1 disrupts pancreatic neuroendocrine tumor development. Oncogene 31: 1459-1467.

Shree T*, Olson OC*, Elie BT, Kester JC, Garfall AL, Simpson K, Bell-McGuinn KM, Zabor EC, Brogi E, and Joyce JA (2011). Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes and Development 25: 2465-2479.

Mason SD and Joyce JA (2011). Proteolytic networks in cancer. Trends in Cell Biology 21: 228-237.

Mason SD and Joyce JA (2011). Proteolytic cascades in invasion and metastasis. Cancer Metastasis: Biologic Basis and Therapeutics. Cambridge University Press. Editors: Lyden DC, Welsh DR, Psaila B.

Wang HW and Joyce JA (2010). Alternative activation of tumor-associated macrophages by IL-4: priming for protumoral functions. Cell Cycle 9: 4824-4835.

Gocheva V*, Wang HW*, Gadea BB, Shree T, Hunter KE, Garfall A, Berman T, and Joyce JA (2010). IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes and Development 24: 241-255.

Gocheva V, Chen X, Peters C, Reinheckel T, and Joyce JA (2010). Deletion of cathepsin H reduces angiogenic switching, tumor vascularization and growth in a mouse model of pancreatic cancer. Biological Chemistry 391: 937-945.

Elie B, Gocheva V, Shree T, Dalrymple SA, Holsinger LJ, and Joyce JA (2010). Identification and preclinical testing of a reversible cathepsin protease inhibitor reveals anti-tumor effects in a pancreatic cancer model. Biochimie 92: 1618-1624.

Joyce JA and Pollard JW (2009). Microenvironmental regulation of metastasis. Nature Reviews Cancer 9: 239-252.

Chang SH, Kanasaki K, Gocheva V, Blum G, Harper J, Moses MA, Shih SC, Manseau EJ, Nagy JA, Joyce JA, Bogyo, M, Kalluri R and Dvorak HF (2009). VEGF-A induces angiogenesis by perturbing the cathepsin-cysteine protease inhibitor balance in venules, causing basement membrane degradation and mother vessel formation. Cancer Research 69: 4537-4544.

Amankulor N, Hambardzumyan D, Pyonteck SM, Becher OJ, Joyce JA and Holland EC (2009). Sonic hedgehog pathway activation is induced by acute brain injury and regulated by injury-related inflammation. Journal of Neuroscience 29: 10299-308.

Reinheckel T, Gocheva V, Peters C and Joyce JA (2008). Roles of cysteine proteases in tumor progression: analysis of cysteine cathepsin knockout mice in cancer models. The Cancer Degradome- Proteases and Cancer Biology. Springer Publishing. Eds. Edwards DR, Hoer-Hansen G, Blasi F, Sloane BF. p. 279-302.

Palermo C and Joyce JA (2008). Cysteine cathepsin proteases as pharmacological targets in cancer. Trends in Pharmacological Sciences 29: 22-28.

Abboud-Jarrous G, Atzmon R, Peretz T, Palermo C, Gadea BB, Joyce JA and Vlodavsky I (2008). Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. Journal of Biological Chemistry 26: 18167-18176.

Gocheva V, Joyce JA (2007). Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 6: 60-64.

Sadaghiani AM, Verhelst SH, Gocheva V, Hill K, Majerova E, Stinson S, Joyce JA, Bogyo M (2007). Design, synthesis, and evaluation of in vivo potency and selectivity of epoxysuccinyl-based inhibitors of papain-family cysteine proteases. Chemistry and Biology 14: 499-511.

Bell-McGuinn K, Garfall A, Bogyo M, Hanahan D, and Joyce JA (2007). Inhibition of cysteine cathepsin protease activity enhances chemotherapy regimens by decreasing tumor growth and invasiveness in a mouse model of multistage cancer. Cancer Research 67: 7378-7385.

Gocheva V, Wei Z, Ke D, Klimstra D, Reinheckel T, Peters C, Hanahan D, Joyce JA (2006). Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes and Development 20: 543-556.

Gadea BB, Joyce JA (2006). Tumour-host interactions: Implications for developing anti-cancer therapies. Expert Rev Mol Med. 8: 1-32.

Joyce JA (2005). Therapeutic targeting of the tumor microenvironment. Cancer Cell 6: 513-520.

Joyce JA, Freeman C, Meyer-Morse N, Parish CR, Hanahan D (2005). A functional heparan sulfate mimetic implicates both heparanase and heparan sulfate in tumor angiogenesis and invasion in a mouse model of multistage cancer. Oncogene 25: 4037-4051.

Joyce JA, Baruch A, Chehade K, Meyer-Morse N, Giraudo E, Tsai, F-Y, Greenbaum D, Hager JH, Bogyo M, Hanahan D (2004). Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 5: 443-453.

Joyce JA, Hanahan D (2004). Multiple roles for cysteine cathepsins in cancer. Cell Cycle 12: 1516-1619.

Joyce JA, Laakkonen P, Bernasconi M, Bergers G, Ruoslahti E, Hanahan D (2003). Stage-specific vascular markers revealed by phage display in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 5: 393-403.