How the microenvironment wires the natural history of chronic lymphocytic leukemia

Seminars in Cancer Biology

Volumn 24, Issue , 2014, Pages 43-48

  Caligaris Cappio, Federico ^a,b   Bertilaccio, Maria T S ^a   Scielzo, Cristina ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Chronic lymphocytic leukemia; Cytoskeleton; Microenviroment; Mouse models

Indexed keywords

DASATINIB; FOSTAMATINIB; IBRUTINIB; IDELALISIB; LENALIDOMIDE;

CANCER GROWTH; CELL HOMING; CELL MIGRATION; CHRONIC LYMPHATIC LEUKEMIA; DISEASE MODEL; DRUG EFFICACY; DRUG SAFETY; HEMATOPOIETIC STEM CELL; HISTORY; HUMAN; LEUKEMIA CELL; LEUKEMOGENESIS; MOLECULAR INTERACTION; MONOCLONAL B CELL LYMPHOCYTOSIS; NONHUMAN; REVIEW; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT;

CHRONIC LYMPHOCYTIC LEUKEMIA; CYTOSKELETON; MICROENVIROMENT; MOUSE MODELS;

ANIMALS; CARCINOGENESIS; CYTOSKELETON; DISEASE MODELS, ANIMAL; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MICE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84892840003     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2013.06.010     Document Type: Review

References (62)

1. Caligaris-Cappio F., Ghia P. Novel insights in chronic lymphocytic leukemia: are we getting closer to understanding the pathogenesis of the diseaseα. Journal of Clinical Oncology 2008, 26:4497-4503.
2. Calissano C., Damle R.N., Hayes G., Murphy E.J., Hellerstein M.K., Moreno C., et al. In vivo intraclonal and interclonal kinetic heterogeneity in B-cell chronic lymphocytic leukemia. Blood 2009, 114:4832-4842.
3. Burger J.A., Tsukada N., Burger M., Zvaifler N.J., Dell'Aquila M., Kipps T.J. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000, 96:2655-2663.
4. Damle R.N., Ghiotto F., Valetto A., Albesiano E., Fais F., Yan X.J., et al. B-cell chronic lymphocytic leukemia cells express a surface membrane phenotype of activated, antigen-experienced B lymphocytes. Blood 2002, 99:4087-4093.
5. Rosen A., Murray F., Evaldsson C., Rosenquist R. Antigens in chronic lymphocytic leukemia-implications for cell origin and leukemogenesis. Seminars in Cancer Biology 2010, 20:400-409.
6. Hoogeboom R., van Kessel K.P., Hochstenbach F., Wormhoudt T.A., Reinten R.J., Wagner K., et al. A mutated B cell chronic lymphocytic leukemia subset that recognizes and responds to fungi. Journal of Experimental Medicine 2013, 210:59-70.
7. Catera R., Silverman G.J., Hatzi K., Seiler T., Didier S., Zhang L., et al. Chronic lymphocytic leukemia cells recognize conserved epitopes associated with apoptosis and oxidation. Molecular Medicine 2008, 14:665-674.
8. Duhren-von Minden M., Ubelhart R., Schneider D., Wossning T., Bach M.P., Buchner M., et al. Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature 2012, 489:309-312.
9. Stevenson F.K., Krysov S., Davies A.J., Steele A.J., Packham G. B-cell receptor signaling in chronic lymphocytic leukemia. Blood 2011, 118:4313-4320.
10. Herishanu Y., Perez-Galan P., Liu D., Biancotto A., Pittaluga S., Vire B., et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood 2011, 117:563-574.
11. Lanham S., Hamblin T., Oscier D., Ibbotson R., Stevenson F., Packham G. Differential signaling via surface IgM is associated with VH gene mutational status and CD38 expression in chronic lymphocytic leukemia. Blood 2003, 101:1087-1093.
12. Muzio M., Apollonio B., Scielzo C., Frenquelli M., Vandoni I., Boussiotis V., et al. Constitutive activation of distinct BCR-signaling pathways in a subset of CLL patients: a molecular signature of anergy. Blood 2008, 112:188-195.
13. Apollonio B., Scielzo C., Bertilaccio M.T., Ten Hacken E., Scarfo L., Ranghetti P., et al. Targeting B cell anergy in chronic lymphocytic leukemia. Blood 2013, 9(121(19)):3879-3888. S1-8.
14. Chiorazzi N., Ferrarini M. B cell chronic lymphocytic leukemia: lessons learned from studies of the B cell antigen receptor. Annual Review of Immunology 2003, 21:841-894.
15. Scielzo C., Bertilaccio M.T., Simonetti G., Dagklis A., ten Hacken E., Fazi C., et al. HS1 has a central role in the trafficking and homing of leukemic B cells. Blood 2010, 116:3537-3546.
16. Granziero L., Ghia P., Circosta P., Gottardi D., Strola G., Geuna M., et al. Survivin is expressed on CD40 stimulation and interfaces proliferation and apoptosis in B-cell chronic lymphocytic leukemia. Blood 2001, 97:2777-2783.
17. Muzio M., Scielzo C., Bertilaccio M.T., Frenquelli M., Ghia P., Caligaris-Cappio F. Expression and function of toll like receptors in chronic lymphocytic leukaemia cells. British Journal of Haematology 2009, 144:507-516.
18. Haiat S., Billard C., Quiney C., Ajchenbaum-Cymbalista F., Kolb J.P. Role of BAFF and APRIL in human B-cell chronic lymphocytic leukaemia. Immunology 2006, 118:281-292.
19. Ntoufa S., Vardi A., Papakonstantinou N., Anagnostopoulos A., Aleporou-Marinou V., Belessi C., et al. Distinct innate immunity pathways to activation and tolerance in subgroups of chronic lymphocytic leukemia with distinct immunoglobulin receptors. Molecular Medicine 2012, 18:1281-1291.
20. Efremov D.G., Bomben R., Gobessi S., Gattei V. TLR9 signaling defines distinct prognostic subsets in CLL. Frontiers in Bioscience: A Journal and Virtual Library 2013, 18:371-386.
21. Liang X., Moseman E.A., Farrar M.A., Bachanova V., Weisdorf D.J., Blazar B.R., et al. Toll-like receptor 9 signaling by CpG-B oligodeoxynucleotides induces an apoptotic pathway in human chronic lymphocytic leukemia B cells. Blood 2010, 115:5041-5052.
22. Muzio M., Bertilaccio M.T., Simonetti G., Frenquelli M., Caligaris-Cappio F. The role of Toll-like receptors in chronic B cell malignancies. Leukemia and Lymphoma 2009, 50(10):1573-1580.
23. Fonte E., Apollonio B., Scarfo L., Ranghetti P., Fazi C., Ghia P., et al. In vitro sensitivity of CLL cells to fludarabine may be modulated by the stimulation of Toll-like receptors. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2013, 19:367-379.
24. Bertilaccio M.T., Simonetti G., Dagklis A., Rocchi M., Rodriguez T.V., Apollonio B., et al. Lack of TIR8/SIGIRR triggers progression of chronic lymphocytic leukemia in mouse models. Blood 2011, 118:660-669.
25. Kikushige Y., Ishikawa F., Miyamoto T., Shima T., Urata S., Yoshimoto G., et al. Self-renewing hematopoietic stem cell is the primary target in pathogenesis of human chronic lymphocytic leukemia. Cancer Cell 2011, 20:246-259.
26. Di Bernardo M.C., Crowther-Swanepoel D., Broderick P., Webb E., Sellick G., Wild R., et al. A genome-wide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nature Genetics 2008, 40:1204-1210.
27. Rawstron A.C., Bennett F.L., O'Connor S.J., Kwok M., Fenton J.A., Plummer M., et al. Monoclonal B-cell lymphocytosis and chronic lymphocytic leukemia. New England Journal of Medicine 2008, 359:575-583.
28. Dagklis A., Fazi C., Scarfo L., Apollonio B., Ghia P. Monoclonal B lymphocytosis in the general population. Leukemia and Lymphoma 2009, 50:490-492.
29. Fazi C., Scarfo L., Pecciarini L., Cottini F., Dagklis A., Janus A., et al. General population low-count CLL-like MBL persists over time without clinical progression, although carrying the same cytogenetic abnormalities of CLL. Blood 2011, 118:6618-6625.
30. Raveche E.S., Smith H., Noguchi P., Chused T.M., Steinberg A.D. Effects of induced anemia in normal and autoimmune mice. Immunological Investigations 1990, 19:307-318.
31. Bichi R., Shinton S.A., Martin E.S., Koval A., Calin G.A., Cesari R., et al. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:6955-6960.
32. Yan X.J., Albesiano E., Zanesi N., Yancopoulos S., Sawyer A., Romano E., et al. B cell receptors in TCL1 transgenic mice resemble those of aggressive, treatment-resistant human chronic lymphocytic leukemia. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:11713-11718.
33. Klein U., Lia M., Crespo M., Siegel R., Shen Q., Mo T., et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 2010, 17:28-40.
34. Wu Q.L., Zierold C., Ranheim E.A. Dysregulation of Frizzled 6 is a critical component of B-cell leukemogenesis in a mouse model of chronic lymphocytic leukemia. Blood 2009, 113:3031-3039.
35. Holler C., Pinon J.D., Denk U., Heyder C., Hofbauer S., Greil R., et al. PKCbeta is essential for the development of chronic lymphocytic leukemia in the TCL1 transgenic mouse model: validation of PKCbeta as a therapeutic target in chronic lymphocytic leukemia. Blood 2009, 113:2791-2794.
36. Enzler T., Kater A.P., Zhang W., Widhopf G.F., Chuang H.Y., Lee J., et al. Chronic lymphocytic leukemia of E{micro}-TCL1 transgenic mice undergoes rapid cell-turnover that can be offset by extrinsic CD257 to accelerate disease progression. Blood 2009, 12(114(20)):4469-4476.
37. Gorgun G., Ramsay A.G., Holderried T.A., Zahrieh D., Le Dieu R., Liu F., et al. E(mu)-TCL1 mice represent a model for immunotherapeutic reversal of chronic lymphocytic leukemia-induced T-cell dysfunction. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6250-6255.
38. Hofbauer J.P., Heyder C., Denk U., Kocher T., Holler C., Trapin D., et al. Development of CLL in the TCL1 transgenic mouse model is associated with severe skewing of the T-cell compartment homologous to human CLL. Leukemia 2011, 25:1452-1458.
39. Tinhofer I., Marschitz I., Kos M., Henn T., Egle A., Villunger A., et al. Differential sensitivity of CD4+ and CD8+ T lymphocytes to the killing efficacy of Fas (Apo-1/CD95) ligand+ tumor cells in B chronic lymphocytic leukemia. Blood 1998, 91:4273-4281.
40. Wu Q.L., Buhtoiarov I.N., Sondel P.M., Rakhmilevich A.L., Ranheim E.A. Tumoricidal effects of activated macrophages in a mouse model of chronic lymphocytic leukemia. Journal of Immunology 2009, 182:6771-6778.
41. Reinart N., Nguyen P.H., Boucas J., Rosen N., Kvasnicka H.M., Heukamp L., et al. Delayed development of chronic lymphocytic leukemia in the absence of macrophage migration inhibitory factor. Blood 2013, 121:812-821.
42. Shimoni A., Marcus H., Canaan A., Ergas D., David M., Berrebi A., et al. A model for human B-chronic lymphocytic leukemia in human/mouse radiation chimera: evidence for tumor-mediated suppression of antibody production in low-stage disease. Blood 1997, 89:2210-2218.
43. Durig J., Ebeling P., Grabellus F., Sorg U.R., Mollmann M., Schutt P., et al. A novel nonobese diabetic/severe combined immunodeficient xenograft model for chronic lymphocytic leukemia reflects important clinical characteristics of the disease. Cancer Research 2007, 67:8653-8661.
44. Bagnara D., Kaufman M.S., Calissano C., Marsilio S., Patten P.E., Simone R., et al. A novel adoptive transfer model of chronic lymphocytic leukemia suggests a key role for T lymphocytes in the disease. Blood 2011, 117:5463-5472.
45. Kurtova A.V., Balakrishnan K., Chen R., Ding W., Schnabl S., Quiroga M.P., et al. Diverse marrow stromal cells protect CLL cells from spontaneous and drug-induced apoptosis: development of a reliable and reproducible system to assess stromal cell adhesion-mediated drug resistance. Blood 2009, 114:4441-4450.
46. Deaglio S., Capobianco A., Bergui L., Durig J., Morabito F., Duhrsen U., et al. CD38 is a signaling molecule in B-cell chronic lymphocytic leukemia cells. Blood 2003, 102:2146-2155.
47. Richardson S.J., Matthews C., Catherwood M.A., Alexander H.D., Carey B.S., Farrugia J., et al. ZAP-70 expression is associated with enhanced ability to respond to migratory and survival signals in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006, 107:3584-3592.
48. Davids M.S., Burger J.A. Cell trafficking in chronic lymphocytic leukemia. Open Journal of Hematology 2012, 3:S1.
49. Hartmann T.N., Grabovsky V., Wang W., Desch P., Rubenzer G., Wollner S., et al. Circulating B-cell chronic lymphocytic leukemia cells display impaired migration to lymph nodes and bone marrow. Cancer Research 2009, 69:3121-3130.
50. Montresor A., Bolomini-Vittori M., Simon S.I., Rigo A., Vinante F., Laudanna C. Comparative analysis of normal versus CLL B-lymphocytes reveals patient-specific variability in signaling mechanisms controlling LFA-1 activation by chemokines. Cancer Research 2009, 69:9281-9290.
51. Till K.J., Harris R.J., Linford A., Spiller D.G., Zuzel M., Cawley J.C. Cell motility in chronic lymphocytic leukemia: defective Rap1 and alphaLbeta2 activation by chemokine. Cancer Research 2008, 68:8429-8436.
52. Stark R.S., Liebes L.F., Shelanski M.L., Silber R. Anomalous function of vimentin in chronic lymphocytic leukemia lymphocytes. Blood 1984, 63:415-420.
53. Caligaris-Cappio F., Bergui L., Tesio L., Corbascio G., Tousco F., Marchisio P.C. Cytoskeleton organization is aberrantly rearranged in the cells of B chronic lymphocytic leukemia and hairy cell leukemia. Blood 1986, 67:233-239.
54. Hao J.J., Zhu J., Zhou K., Smith N., Zhan X. The coiled-coil domain is required for HS1 to bind to F-actin and activate Arp2/3 complex. Journal of Biological Chemistry 2005, 280:37988-37994.
55. Sanchez-Aguilera A., Rattmann I., Drew D.Z., Muller L.U., Summey V., Lucas D.M., et al. Involvement of RhoH GTPase in the development of B-cell chronic lymphocytic leukemia. Leukemia 2010, 24:97-104.
56. Scielzo C., Bertilaccio M.T., Simonetti G., Dagklis A., ten Hacken E., Fazi C., et al. HS1 has a central role in the trafficking and homing of leukemic B cells. Blood 2010, 116:3537-3546.
57. Gomez T.S., McCarney S.D., Carrizosa E., Labno C.M., Comiskey E.O., Nolz J.C., et al. HS1 functions as an essential actin-regulatory adaptor protein at the immune synapse. Immunity 2006, 24:741-752.
58. Ten Hacken E., Scielzo C., Bertilaccio M.T., Scarfo L., Apollonio B., Barbaglio F., et al. Targeting the LYN/HS1 signaling axis in chronic lymphocytic leukemia. Blood 2013, 21(121(12)):2264-2313.
59. Woyach J.A., Johnson A.J., Byrd J.C. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood 2012, 120:1175-1184.
60. Young R.M., Staudt L.M. Targeting pathological B cell receptor signalling in lymphoid malignancies. Nature Reviews. Drug Discovery 2013, 12:229-243.
61. Tai Y.T., Chang B.Y., Kong S.Y., Fulciniti M., Yang G., Calle Y., et al. Bruton tyrosine kinase inhibition is a novel therapeutic strategy targeting tumor in the bone marrow microenvironment in multiple myeloma. Blood 2012, 120:1877-1887.
62. Hallek M., Cheson B.D., Catovsky D., Caligaris-Cappio F., Dighiero G., Dohner H., et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008, 111:5446-5456.