Colony-stimulating factor-1 receptor is required for nurse-like cell survival in chronic lymphocytic leukemia

Clinical Cancer Research

Volumn 22, Issue 24, 2016, Pages 6118-6128

  Polk, Avery ^a   Lu, Ye ^a   Wang, Tianjiao ^a   Seymour, Erlene ^a   Bailey, Nathanael G ^a   Singer, Jack W ^b   Boonstra, Philip S ^c   Lim, Megan S ^d   Malek, Sami ^a   Wilcox, Ryan A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CTI BioPharma   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; COLONY STIMULATING FACTOR 1 RECEPTOR; COLONY STIMULATING FACTOR RECEPTOR; FEDRATINIB; FLT3 LIGAND; JANUS KINASE 2; PACRITINIB; PROTEIN TYROSINE KINASE INHIBITOR; RUXOLITINIB; UNCLASSIFIED DRUG; CSF1R PROTEIN, HUMAN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL GROWTH; CELL MOTILITY; CELL SURVIVAL; CELL VIABILITY; CHRONIC LYMPHATIC LEUKEMIA; CONCENTRATION RESPONSE; CSF 1 GENE; DRUG EFFICACY; DRUG MECHANISM; GENE; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; IC50; LYMPHOCYTE PROLIFERATION; MACROPHAGE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TUMOR MICROENVIRONMENT; CELL PROLIFERATION; DRUG EFFECTS; METABOLISM; MONOCYTE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

B-LYMPHOCYTES; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MACROPHAGES; MONOCYTES; PROTEIN KINASE INHIBITORS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION;

EID: 85006993289     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-3099     Document Type: Article

References (56)

1. Wilcox RA. Cancer-associated myeloproliferation: old association, new therapeutic target. Mayo Clin Proc 2010;85:656-63.
2. Coscia M, Pantaleoni F, Riganti C, Vitale C, Rigoni M, Peola S, et al. IGHV unmutated CLL B cells are more prone to spontaneous apoptosis and subject to environmental prosurvival signals than mutated CLL B cells. Leukemia 2011;25:828-37.
3. Seiffert M, Schulz A, Ohl S, Dohner H, Stilgenbauer S, Lichter P. Soluble CD14 is a novel monocyte-derived survival factor for chronic lymphocytic leukemia cells, which is induced by CLL cells in vitro and present at abnormally high levels in vivo. Blood 2010;116:4223-30.
4. Reinart N, Nguyen PH, Boucas J, Rosen N, Kvasnicka HM, Heukamp L, et al. Delayed development of chronic lymphocytic leukemia in the absence of macrophage migration inhibitory factor. Blood 2013;121:812-21.
5. Zucchetto A, Benedetti D, Tripodo C, Bomben R, Dal Bo M, Marconi D, et al. CD38/CD31, the CCL3 and CCL4 chemokines, and CD49d/vascular cell adhesion molecule-1 are interchained by sequential events sustaining chronic lymphocytic leukemia cell survival. Cancer Res 2009;69:4001-9.
6. Hanna BS, McClanahan F, Yazdanparast H, Zaborsky N, Kalter V, Rossner P, et al. Depletion of CLL-associated patrolling monocytes and macrophages controls disease development and repairs immune dysfunction in vivo. Leukemia 2016;30:570-9.
7. Mueller CG, Boix C, Kwan WH, Daussy C, Fournier E, Fridman WH, et al. Critical role of monocytes to support normal B cell and diffuse large B cell lymphoma survival and proliferation. J Leukoc Biol 2007;82:567-75.
8. Friedman DR, Sibley AB, Owzar K, Chaffee KG, Slager S, Kay NE, et al. Relationship of blood monocytes with chronic lymphocytic leukemia aggressiveness and outcomes: a multi-institutional study. Am J Hematol 2016;91:687-91.
9. Herishanu Y, Kay S, Sarid N, Kohan P, Braunstein R, Rotman R, et al. Absolute monocyte count trichotomizes chronic lymphocytic leukemia into high risk patients with immune dysregulation, disease progression and poor survival. Leuk Res 2013;37:1222-8.
10. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, Kipps TJ. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000;96:2655-63.
11. Bhattacharya N, Diener S, Idler IS, Rauen J, Habe S, Busch H, et al. Nurse-like cells show deregulated expression of genes involved in immunocompetence. Br J Haematol 2011;154:349-56.
12. Tsukada N, Burger JA, Zvaifler NJ, Kipps TJ. Distinctive features of "nurse-like" cells that differentiate in the context of chronic lymphocytic leukemia. Blood 2002;99:1030-7.
13. Ysebaert L, Fournie JJ. Genomic and phenotypic characterization of nurse-like cells that promote drug resistance in chronic lymphocytic leukemia. Leuk Lymphoma 2011;52:1404-6.
14. Filip AA, Cisel B, Koczkodaj D, Wasik-Szczepanek E, Piersiak T, Dmoszynska A. Circulating microenvironment of CLL: are nurse-like cells related to tumor-associated macrophages? Blood Cells Mol Dis 2013;50:263-70.
15. Wang T, Feldman AL, Wada DA, Lu Y, Polk A, Briski R, et al. GATA-3 expression identifies a high-risk subset of PTCL, NOS with distinct molecular and clinical features. Blood 2014;123:3007-15.
16. Wilcox RA, Wada DA, Ziesmer SC, Elsawa SF, Comfere NI, Dietz AB, et al. Monocytes promote tumor cell survival in T-cell lymphoproliferative disorders and are impaired in their ability to differentiate into mature dendritic cells. Blood 2009;114:2936-44.
17. Wang T, Feldman AL, Wada DA, Lu Y, Polk A, Briski R, et al. GATA-3 expression promotes IL-10 production, alternative macrophage polarization, and identifies a subset of high-risk PTCL, NOS [abstract]. In: Proceedings of the 55th ASH Annual Meeting and Exposition; 2013 Dec 7-10; New Orleans, LA. Washington, DC: ASH; 2013. Abstract nr 841.
18. Cecchini MG, Dominguez MG, Mocci S, Wetterwald A, Felix R, Fleisch H, et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 1994;120:1357-72.
19. Marks SC Jr, Lane PW. Osteopetrosis, a new recessive skeletal mutation on chromosome 12 of the mouse. J Hered 1976;67:11-8.
20. Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW Jr, Ahmed-Ansari A, Sell KW, Pollard JW, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A 1990;87:4828-32.
21. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 1990;345:442-4.
22. Zhang M, Xu CR, Shamiyeh E, Liu F, Yin J, von Moltke LL, et al. A randomized, placebo-controlled study of the pharmacokinetics, pharmacodynamics, and tolerability of the oral JAK2 inhibitor fedratinib (SAR302503) in healthy volunteers. J Clin Pharmacol 2014;54:415-21.
23. Haegel H, Thioudellet C, Hallet R, Geist M, Menguy T, Le Pogam F, et al. A unique anti-CD115 monoclonal antibody which inhibits osteolysis and skews human monocyte differentiation from M2-polarized macrophages toward dendritic cells. mAbs 2013;5:736-47.
24. Anastassiadis T, Deacon SW, Devarajan K, Ma H, Peterson JR. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat Biotechnol 2011;29:1039-45.
25. Friedman DR, Weinberg JB, Barry WT, Goodman BK, Volkheimer AD, Bond KM, et al. A genomic approach to improve prognosis and predict therapeutic response in chronic lymphocytic leukemia. Clin Cancer Res 2009;15:6947-55.
26. MacDonald KP, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood 2010;116:3955-63.
27. DiLillo DJ, Weinberg JB, Yoshizaki A, Horikawa M, Bryant JM, Iwata Y, et al. Chronic lymphocytic leukemia and regulatory B cells share IL-10 competence and immunosuppressive function. Leukemia 2013;27:170-82.
28. Lai R, O'Brien S, Maushouri T, Rogers A, Kantarjian H, Keating M, et al. Prognostic value of plasma interleukin-6 levels in patients with chronic lymphocytic leukemia. Cancer 2002;95:1071-5.
29. Chomarat P, Banchereau J, Davoust J, Palucka AK. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 2000;1:510-4.
30. Saulep-Easton D, Vincent FB, Quah PS, Wei A, Ting SB, Croce CM, et al. The BAFF receptor TACI controls IL-10 production by regulatory B cells and CLL B cells. Leukemia 2016;30:163-72.
31. Bartocci A, Mastrogiannis DS, Migliorati G, Stockert RJ, Wolkoff AW, Stanley ER. Macrophages specifically regulate the concentration of their own growth factor in the circulation. Proc Natl Acad Sci U S A 1987;84:6179-83.
32. Byrd JC, Brown JR, O'Brien S, Barrientos JC, Kay NE, Reddy NM, et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med 2014;371:213-23.
33. Byrd JC, O'Brien S, James DF. Ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med 2013;369:1278-9.
34. ten Hacken E, Burger JA. Molecular pathways: targeting the microenvironment in chronic lymphocytic leukemia-focus on the B-cell receptor. Clin Cancer Res 2014;20:548-56.
35. Niemann CU, Herman SE, Maric I, Gomez-Rodriguez J, Biancotto A, Chang BY, et al. Disruption of in vivo chronic lymphocytic leukemia tumor-microenvironment interactions by ibrutinib - findings from an investigator initiated phase 2 study. Clin Cancer Res 2016;22:1572-82.
36. Mok S, Koya RC, Tsui C, Xu J, Robert L, Wu L, et al. Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res 2014;74:153-61.
37. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013;19:1264-72.
38. Zhu Y, Knolhoff BL, Meyer MA, Nywening TM, West BL, Luo J, et al. CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res 2014;74:5057-69.
39. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011;332:1284-8.
40. Zhou T, Georgeon S, Moser R, Moore DJ, Caflisch A, Hantschel O. Specificity and mechanism-of-action of the JAK2 tyrosine kinase inhibitors ruxolitinib and SAR302503 (TG101348). Leukemia 2014;28:404-7.
41. Pixley FJ, Stanley ER. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol 2004;14:628-38.
42. Herman SE, Gordon AL, Hertlein E, Ramanunni A, Zhang X, Jaglowski S, et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood 2011;117:6287-96.
43. Wilcox RA, Ristow K, Habermann TM, Inwards DJ, Micallef IN, Johnston PB, et al. The absolute monocyte and lymphocyte prognostic score predicts survival and identifies high-risk patients in diffuse large-B-cell lymphoma. Leukemia 2011;25:1502-9.
44. Burger JA. Targeting the microenvironment in chronic lymphocytic leukemia is changing the therapeutic landscape. Curr Opin Oncol 2012;24:643-9.
45. Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, et al. Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell 2013;23:249-62.
46. Radi ZA, Koza-Taylor PH, Bell RR, Obert LA, Runnels HA, Beebe JS, et al. Increased serum enzyme levels associated with kupffer cell reduction with no signs of hepatic or skeletal muscle injury. Am J Pathol 2011;179:240-7.
47. Cassier PA, Italiano A, Gomez-Roca CA, Le Tourneau C, Toulmonde M, Cannarile MA, et al. CSF1R inhibition with emactuzumab in locally advanced diffuse-type tenosynovial giant cell tumours of the soft tissue: a dose-escalation and dose-expansion phase 1 study. Lancet Oncol 2015;16:949-56.
48. Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 2014;25:846-59.
49. Hume DA, MacDonald KP. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 2012;119:1810-20.
50. Breen FN, Hume DA, Weidemann MJ. Interactions among granulocyte-macrophage colony-stimulating factor, macrophage colony-stimulating factor, and IFN-gamma lead to enhanced proliferation of murine macrophage progenitor cells. J Immunol 1991;147:1542-7.
51. Younes A, Romaguera J, Fanale M, McLaughlin P, Hagemeister F, Copeland A, et al. Phase I study of a novel oral Janus kinase 2 inhibitor, SB1518, in patients with relapsed lymphoma: evidence of clinical and biologic activity in multiple lymphoma subtypes. J Clin Oncol 2012;30:4161-7.
52. Wang T, Feldman AL, Wada DA, Lu Y, Polk A, Briski R, et al. GATA-3 expression identifies a high-risk subset of PTCL, NOS with distinct molecular and clinical features. Blood 2014;123:3007-15.
53. Rozovski U, Wu JY, Harris DM, Liu Z, Li P, Hazan-Halevy I, et al. Stimulation of the B-cell receptor activates the JAK2/STAT3 signaling pathway in chronic lymphocytic leukemia cells. Blood 2014;123:3797-802.
54. Kitabayashi A, Hirokawa M, Miura AB. The role of interleukin-10 (IL-10) in chronic B-lymphocytic leukemia: IL-10 prevents leukemic cells from apoptotic cell death. Int J Hematol 1995;62:99-106.
55. Steele AJ, Prentice AG, Cwynarski K, Hoffbrand AV, Hart SM, Lowdell MW, et al. The JAK3-selective inhibitor PF-956980 reverses the resistance to cytotoxic agents induced by interleukin-4 treatment of chronic lymphocytic leukemia cells: potential for reversal of cytoprotection by the microenvironment. Blood 2010;116:4569-77.
56. Hatzimichael E, Tsolas E, Briasoulis E. Profile of pacritinib and its potential in the treatment of hematologic disorders. J Blood Med 2014;5:143-52.