Multiple metamorphoses of CD38 from prognostic marker to disease modifier to therapeutic target in chronic lymphocytic leukemia

Current Topics in Medicinal Chemistry

Volumn 13, Issue 23, 2013, Pages 2955-2964

  Vaisitti, Tiziana ^a   Audrito, Valentina ^a   Serra, Sara ^a   Bologna, Cinzia ^a   Arruga, Francesca ^a   Brusa, Davide ^a   Buonincontri, Roberta ^a   Gizdic, Branimir ^a   Deaglio, Silvia ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

CD38; Chronic lymphocytic leukemia; Ecto enzymes; Homing; Microenvironment; Therapeutic target

Indexed keywords

CD38 ANTIGEN; DARATUMUMAB; INTEGRIN; LENALIDOMIDE; MATRIX METALLOPROTEINASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD38; MOR 03087; PROTEIN KINASE ZAP 70; RITUXIMAB; SAR 650984; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CELL ADHESION; CELL HOMING; CELL PROLIFERATION; CHEMOTAXIS; CHRONIC LYMPHATIC LEUKEMIA; COMPLEMENT DEPENDENT CYTOTOXICITY; DISEASE COURSE; DISEASE MARKER; DRUG TARGETING; GENE EXPRESSION; HUMAN; LEUKEMIA CELL; MULTIPLE MYELOMA; NONHUMAN; SIGNAL TRANSDUCTION;

ANTIGENS, CD38; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MEMBRANE GLYCOPROTEINS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84889042527     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/15680266113136660210     Document Type: Article

References (109)

1. Chan, C. S.; Wormsley, S. B.; Pierce, L. E.; Peter, J. B.; Schechter, G. P., B-cell surface phenotypes of proliferating myeloma cells: target antigens for immunotherapy. Am. J. Hematol., 1990, 33(2), 101-109.
2. Hoffmann, C.; Tiemann, M.; Schrader, C.; Janssen, D.; Wolf, E.; Vierbuchen, M.; Parwaresch, R.; Ernestus, K.; Plettenberg, A.; Stoehr, A.; Fatkenheuer, G.; Wyen, C.; Oette, M.; Horst, H. A., AIDS-related B-cell lymphoma (ARL): correlation of prognosis with differentiation profiles assessed by immunophenotyping. Blood, 2005, 106(5), 1762-1769.
3. Rochford, R.; Hobbs, M. V.; Garnier, J. L.; Cooper, N. R.; Cannon, M. J., Plasmacytoid differentiation of Epstein-Barr virustransformed B cells in vivo is associated with reduced expression of viral latent genes. Proc. Natl. Acad. Sci. U. S. A., 1993, 90(1), 352-356.
4. Reinherz, E. L.; Kung, P. C.; Goldstein, G.; Levey, R. H.; Schlossman, S. F., Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc. Natl. Acad. Sci. U. S. A., 1980, 77(3), 1588-1592.
5. Malavasi, F.; Deaglio, S.; Funaro, A.; Ferrero, E.; Horenstein, A. L.; Ortolan, E.; Vaisitti, T.; Aydin, S., Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol. Rev., 2008, 88(3), 841-886.
6. Funaro, A.; Spagnoli, G. C.; Ausiello, C. M.; Alessio, M.; Roggero, S.; Delia, D.; Zaccolo, M.; Malavasi, F., Involvement of the multilineage CD38 molecule in a unique pathway of cell activation and proliferation. J. Immunol., 1990, 145(8), 2390-2396.
7. Kitanaka, A.; Ito, C.; Coustan-Smith, E.; Campana, D., CD38 ligation in human B cell progenitors triggers tyrosine phosphorylation of CD19 and association of CD19 with lyn and phosphatidylinositol 3-kinase. J. Immunol., 1997, 159(1), 184-192.
8. Zubiaur, M.; Izquierdo, M.; Terhorst, C.; Malavasi, F.; Sancho, J., CD38 ligation results in activation of the Raf-1/mitogen-activated protein kinase and the CD3-zeta/zeta-associated protein-70 signaling pathways in Jurkat T lymphocytes. J. Immunol., 1997, 159(1), 193-205.
9. Moreno-Garcia, M. E.; Lopez-Bojorques, L. N.; Zentella, A.; Humphries, L. A.; Rawlings, D. J.; Santos-Argumedo, L., CD38 signaling regulates B lymphocyte activation via a phospholipase C (PLC)-gamma 2-independent, protein kinase C, phosphatidylcholine-PLC, and phospholipase D-dependent signaling cascade. J. Immunol., 2005, 174(5), 2687-2695.
10. Musso, T.; Deaglio, S.; Franco, L.; Calosso, L.; Badolato, R.; Garbarino, G.; Dianzani, U.; Malavasi, F., CD38 expression and functional activities are up-regulated by IFN-gamma on human monocytes and monocytic cell lines. J. Leukoc. Biol., 2001, 69(4), 605-612.
11. Munshi, C.; Baumann, C.; Levitt, D.; Bloomfield, V. A.; Lee, H. C., The homo-dimeric form of ADP-ribosyl cyclase in solution. Biochim. Biophys. Acta, 1998, 1388(2), 428-436.
12. Hara-Yokoyama, M.; Kukimoto-Niino, M.; Terasawa, K.; Harumiya, S.; Podyma-Inoue, K. A.; Hino, N.; Sakamoto, K.; Itoh, S.; Hashii, N.; Hiruta, Y.; Kawasaki, N.; Mishima-Tsumagari, C.; Kaitsu, Y.; Matsumoto, T.; Wakiyama, M.; Shirouzu, M.; Kasama, T.; Takayanagi, H.; Utsunomiya-Tate, N.; Takatsu, K.; Katada, T.; Hirabayashi, Y.; Yokoyama, S.; Yanagishita, M., Tetrameric interaction of the ectoenzyme CD38 on the cell surface enables its catalytic and raft-association activities. Structure, 2012, 20(9), 1585-1595.
13. Deaglio, S.; Vaisitti, T.; Billington, R.; Bergui, L.; Omede, P.; Genazzani, A. A.; Malavasi, F., CD38/CD19: a lipid raft-dependent signaling complex in human B cells. Blood, 2007, 109(12), 5390-5398.
14. Morra, M.; Zubiaur, M.; Terhorst, C.; Sancho, J.; Malavasi, F., CD38 is functionally dependent on the TCR/CD3 complex in human T cells. FASEB J., 1998, 12(7), 581-592.
15. Zubiaur, M.; Fernandez, O.; Ferrero, E.; Salmeron, J.; Malissen, B.; Malavasi, F.; Sancho, J., CD38 is associated with lipid rafts and upon receptor stimulation leads to Akt/protein kinase B and Erk activation in the absence of the CD3-zeta immune receptor tyrosinebased activation motifs. J. Biol. Chem., 2002, 277(1), 13-22.
16. Munoz, P.; Navarro, M. D.; Pavon, E. J.; Salmeron, J.; Malavasi, F.; Sancho, J.; Zubiaur, M., CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-zeta subunit of the T cell antigen receptor. J. Biol. Chem., 2003, 278(50), 50791-50802.
17. Fedele, G.; Frasca, L.; Palazzo, R.; Ferrero, E.; Malavasi, F.; Ausiello, C. M., CD38 is expressed on human mature monocytederived dendritic cells and is functionally involved in CD83 expression and IL-12 induction. Eur. J. Immunol., 2004, 34(5), 1342-1350.
18. Dianzani, U.; Funaro, A.; DiFranco, D.; Garbarino, G.; Bragardo, M.; Redoglia, V.; Buonfiglio, D.; De Monte, L. B.; Pileri, A.; Malavasi, F., Interaction between endothelium and CD4+CD45RA+ lymphocytes. Role of the human CD38 molecule. J. Immunol., 1994, 153(3), 952-959.
19. Deaglio, S.; Dianzani, U.; Horenstein, A. L.; Fernandez, J. E.; van Kooten, C.; Bragardo, M.; Funaro, A.; Garbarino, G.; Di Virgilio, F.; Banchereau, J.; Malavasi, F., Human CD38 ligand. A 120-KDA protein predominantly expressed on endothelial cells. J. Immunol., 1996, 156(2), 727-734.
20. Deaglio, S.; Morra, M.; Mallone, R.; Ausiello, C. M.; Prager, E.; Garbarino, G.; Dianzani, U.; Stockinger, H.; Malavasi, F., Human CD38 (ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J. Immunol., 1998, 160(1), 395-402.
21. Howard, M.; Grimaldi, J. C.; Bazan, J. F.; Lund, F. E.; Santos-Argumedo, L.; Parkhouse, R. M.; Walseth, T. F.; Lee, H. C., Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science, 1993, 262(5136), 1056-1059.
22. States, D. J.; Walseth, T. F.; Lee, H. C., Similarities in amino acid sequences of Aplysia ADP-ribosyl cyclase and human lymphocyte antigen CD38. Trends Biochem. Sci., 1992, 17(12), 495.
23. Aarhus, R.; Graeff, R. M.; Dickey, D. M.; Walseth, T. F.; Lee, H. C., ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calciummobilizing metabolite from NADP. J. Biol. Chem., 1995, 270(51), 30327-30333.
24. Graeff, R.; Liu, Q.; Kriksunov, I. A.; Hao, Q.; Lee, H. C., Acidic residues at the active sites of CD38 and ADP-ribosyl cyclase determine nicotinic acid adenine dinucleotide phosphate (NAADP) synthesis and hydrolysis activities. J. Biol. Chem., 2006, 281(39), 28951-28957.
25. Prasad, G. S.; McRee, D. E.; Stura, E. A.; Levitt, D. G.; Lee, H. C.; Stout, C. D., Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectozyme CD38. Nat. Struct. Biol., 1996, 3(11), 957-964.
26. Liu, Q.; Kriksunov, I. A.; Graeff, R.; Munshi, C.; Lee, H. C.; Hao, Q., Crystal structure of human CD38 extracellular domain. Structure, 2005, 13(9), 1331-1339.
27. Munshi, C.; Aarhus, R.; Graeff, R.; Walseth, T. F.; Levitt, D.; Lee, H. C., Identification of the enzymatic active site of CD38 by sitedirected mutagenesis. J. Biol. Chem., 2000, 275(28), 21566-21571.
28. Munshi, C.; Thiel, D. J.; Mathews, II; Aarhus, R.; Walseth, T. F.; Lee, H. C., Characterization of the active site of ADP-ribosyl cyclase. J. Biol. Chem., 1999, 274(43), 30770-30777.
29. Deaglio, S.; Malavasi, F., The CD38/CD157 mammalian gene family: an evolutionary paradigm for other leukocyte surface enzymes. Purinergic Signal., 2006, 2, 431-441.
30. Di Virgilio, F., Purines, purinergic receptors, and cancer. Cancer Res., 2012, 72(21), 5441-5447.
31. Goding, J. W.; Howard, M. C., Ecto-enzymes of lymphoid cells. Immunol. Rev., 1998, 161, 5-10.
32. Fredholm, B. B.; AP, I. J.; Jacobson, K. A.; Klotz, K. N.; Linden, J., International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev., 2001, 53(4), 527-552.
33. Burnstock, G., Introduction: P2 receptors. Curr. Top. Med. Chem., 2004, 4(8), 793-803.
34. Liu, Q.; Graeff, R.; Kriksunov, I. A.; Jiang, H.; Zhang, B.; Oppenheimer, N.; Lin, H.; Potter, B. V.; Lee, H. C.; Hao, Q., Structural basis for enzymatic evolution from a dedicated ADP-ribosyl cyclase to a multifunctional NAD hydrolase. J. Biol. Chem., 2009, 284(40), 27637-27645.
35. Chiorazzi, N.; Rai, K. R.; Ferrarini, M., Chronic lymphocytic leukemia. N. Engl. J. Med., 2005, 352(8), 804-815.
36. Hallek, M.; Cheson, B. D.; Catovsky, D.; Caligaris-Cappio, F.; Dighiero, G.; Dohner, H.; Hillmen, P.; Keating, M. J.; Montserrat, E.; Rai, K. R.; Kipps, T. J., Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia (IWCLL) updating the National Cancer Institute-Working Group (NCI-WG) 1996 guidelines. Blood, 2008, 111(12), 5446-56.
37. Zenz, T.; Mertens, D.; Kuppers, R.; Dohner, H.; Stilgenbauer, S., From pathogenesis to treatment of chronic lymphocytic leukaemia. Nat. Rev. Cancer., 2010, 10(1), 37-50.
38. Pleyer, L.; Egle, A.; Hartmann, T. N.; Greil, R., Molecular and cellular mechanisms of CLL: novel therapeutic approaches. Nat. Rev. Clin. Oncol., 2009, 6(7), 405-418.
39. Rossi, D.; Spina, V.; Forconi, F.; Capello, D.; Fangazio, M.; Rasi, S.; Martini, M.; Gattei, V.; Ramponi, A.; Larocca, L. M.; Bertoni, F.; Gaidano, G., Molecular history of Richter syndrome: origin from a cell already present at the time of chronic lymphocytic leukemia diagnosis. Int. J. Cancer, 2012, 130(12), 3006-3010.
40. Dal Bo, M.; Bomben, R.; Zucchetto, A.; Del Poeta, G.; Gaidano, G.; Deaglio, S.; Efremov, D. G.; Gattei, V., Microenvironmental interactions in chronic lymphocytic leukemia: hints for pathogenesis and identification of targets for rational therapy. Curr. Pharm. Des., 2012, 18(23), 3323-3334.
41. Ghia, P.; Chiorazzi, N.; Stamatopoulos, K., Microenvironmental influences in chronic lymphocytic leukaemia: the role of antigen stimulation. J. Intern. Med., 2008, 264(6), 549-562.
42. Burger, J. A., Targeting the microenvironment in chronic lymphocytic leukemia is changing the therapeutic landscape. Curr. Opin. Oncol., 2012, 24(6), 643-649.
43. Caligaris-Cappio, F.; Ghia, P., Novel insights in chronic lymphocytic leukemia: are we getting closer to understanding the pathogenesis of the disease? J. Clin. Oncol., 2008, 26(27), 4497-4503.
44. Damle, R. N.; Wasil, T.; Fais, F.; Ghiotto, F.; Valetto, A.; Allen, S. L.; Buchbinder, A.; Budman, D.; Dittmar, K.; Kolitz, J.; Lichtman, S. M.; Schulman, P.; Vinciguerra, V. P.; Rai, K. R.; Ferrarini, M.; Chiorazzi, N., Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood, 1999, 94(6), 1840-1847.
45. Del Poeta, G.; Maurillo, L.; Venditti, A.; Buccisano, F.; Epiceno, A. M.; Capelli, G.; Tamburini, A.; Suppo, G.; Battaglia, A.; Del Principe, M. I.; Del Moro, B.; Masi, M.; Amadori, S., Clinical significance of CD38 expression in chronic lymphocytic leukemia. Blood, 2001, 98(9), 2633-2639.
46. Durig, J.; Naschar, M.; Schmucker, U.; Renzing-Kohler, K.; Holter, T.; Huttmann, A.; Duhrsen, U., CD38 expression is an important prognostic marker in chronic lymphocytic leukaemia. Leukemia, 2002, 16(1), 30-35.
47. Ibrahim, S.; Keating, M.; Do, K. A.; O'Brien, S.; Huh, Y. O.; Jilani, I.; Lerner, S.; Kantarjian, H. M.; Albitar, M., CD38 expression as an important prognostic factor in B-cell chronic lymphocytic leukemia. Blood, 2001, 98(1), 181-186.
48. Damle, R. N.; Batliwalla, F. M.; Ghiotto, F.; Valetto, A.; Albesiano, E.; Sison, C.; Allen, S. L.; Kolitz, J.; Vinciguerra, V. P.; Kudalkar, P.; Wasil, T.; Rai, K. R.; Ferrarini, M.; Gregersen, P. K.; Chiorazzi, N., Telomere length and telomerase activity delineate distinctive replicative features of the B-CLL subgroups defined by immunoglobulin V gene mutations. Blood, 2004, 103(2), 375-382.
49. Damle, R. N.; Temburni, S.; Calissano, C.; Yancopoulos, S.; Banapour, T.; Sison, C.; Allen, S. L.; Rai, K. R.; Chiorazzi, N., CD38 expression labels an activated subset within chronic lymphocytic leukemia clones enriched in proliferating B cells. Blood, 2007, 110(9), 3352-3359.
50. Lin, T. T.; Hewamana, S.; Ward, R.; Taylor, H.; Payne, T.; Pratt, G.; Baird, D.; Fegan, C.; Pepper, C., Highly purified CD38 subpopulations show no evidence of preferential clonal evolution despite having increased proliferative activity when compared with CD38 sub-populations derived from the same chronic lymphocytic leukaemia patient. Br. J. Haematol., 2008, 142(4), 595-605.
51. Palacios, F.; Moreno, P.; Morande, P.; Abreu, C.; Correa, A.; Porro, V.; Landoni, A. I.; Gabus, R.; Giordano, M.; Dighiero, G.; Pritsch, O.; Oppezzo, P., High expression of AID and active class switch recombination might account for a more aggressive disease in unmutated CLL patients: link with an activated microenvironment in CLL disease. Blood, 2010, 115(22), 4488-4496.
52. Calissano, C.; Damle, R. N.; Hayes, G.; Murphy, E. J.; Hellerstein, M. K.; Moreno, C.; Sison, C.; Kaufman, M. S.; Kolitz, J. E.; Allen, S. L.; Rai, K. R.; Chiorazzi, N., In vivo intraclonal and interclonal kinetic heterogeneity in B-cell chronic lymphocytic leukemia. Blood, 2009, 114(23), 4832-4842.
53. Cramer, P.; Hallek, M., Prognostic factors in chronic lymphocytic leukemia-what do we need to know? Nat. Rev. Clin. Oncol., 2011, 8(1), 38-47.
54. Krober, A.; Seiler, T.; Benner, A.; Bullinger, L.; Bruckle, E.; Lichter, P.; Dohner, H.; Stilgenbauer, S., V(H) mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood, 2002, 100(4), 1410-1416.
55. Braggio, E.; Kay, N. E.; VanWier, S.; Tschumper, R. C.; Smoley, S.; Eckel-Passow, J. E.; Sassoon, T.; Barrett, M.; Van Dyke, D. L.; Byrd, J. C.; Jelinek, D. F.; Shanafelt, T. D.; Fonseca, R., Longitudinal genome-wide analysis of patients with chronic lymphocytic leukemia reveals complex evolution of clonal architecture at disease progression and at the time of relapse. Leukemia, 2012, 26(7), 1698-1701.
56. Gunnarsson, R.; Mansouri, L.; Isaksson, A.; Goransson, H.; Cahill, N.; Jansson, M.; Rasmussen, M.; Lundin, J.; Norin, S.; Buhl, A. M.; Smedby, K. E.; Hjalgrim, H.; Karlsson, K.; Jurlander, J.; Geisler, C.; Juliusson, G.; Rosenquist, R., Array-based genomic screening at diagnosis and during follow-up in chronic lymphocytic leukemia. Haematologica, 2011, 96(8), 1161-1169.
57. Ottaggio, L.; Viaggi, S.; Zunino, A.; Zupo, S.; Rossi, E.; Spriano, M.; Abbondandolo, A.; Ferrarini, M., Chromosome aberrations evaluated by comparative genomic hybridization in B-cell chronic lymphocytic leukemia: correlation with CD38 expression. Haematologica, 2003, 88(7), 769-777.
58. Ouillette, P.; Collins, R.; Shakhan, S.; Li, J.; Peres, E.; Kujawski, L.; Talpaz, M.; Kaminski, M.; Li, C.; Shedden, K.; Malek, S. N., Acquired genomic copy number aberrations and survival in chronic lymphocytic leukemia. Blood, 2011, 118(11), 3051-3061.
59. Calissano, C.; Damle, R. N.; Yan, X. J.; Li, W.; Marsilio, S.; Kolitz, J. E.; Kaufman, M. S.; Allen, S. L.; Rai, K. R.; Chiorazzi, N., Multiparameter phenotypic analysis of members of chronic lymphocytic leukemia clones identifies distinct proliferative and resting/re-entry compartments with discrete gene expression prolfiles. Blood, 2009, 114(22), 279.
60. Pepper, C.; Ward, R.; Lin, T. T.; Brennan, P.; Starczynski, J.; Musson, M.; Rowntree, C.; Bentley, P.; Mills, K.; Pratt, G.; Fegan, C., Highly purified CD38(+) and CD38(-) sub-clones derived from the same chronic lymphocytic leukemia patient have distinct gene expression signatures despite their monoclonal origin. Leukemia, 2007, 21(4), 687-96.
61. Deaglio, S.; Capobianco, A.; Bergui, L.; Durig, J.; Morabito, F.; Duhrsen, U.; Malavasi, F., CD38 is a signaling molecule in B-cell chronic lymphocytic leukemia cells. Blood, 2003, 102(6), 2146-2155.
62. 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(8), 2655-2663.
63. Deaglio, S.; Vaisitti, T.; Bergui, L.; Bonello, L.; Horenstein, A. L.; Tamagnone, L.; Boumsell, L.; Malavasi, F., CD38 and CD100 lead a network of surface receptors relaying positive signals for B-CLL growth and survival. Blood, 2005, 105(8), 3042-3050.
64. Crespo, M.; Bosch, F.; Villamor, N.; Bellosillo, B.; Colomer, D.; Rozman, M.; Marce, S.; Lopez-Guillermo, A.; Campo, E.; Montserrat, E., ZAP-70 expression as a surrogate for immunoglobulinvariable-region mutations in chronic lymphocytic leukemia. N. Engl. J. Med., 2003, 348(18), 1764-1775.
65. Deaglio, S.; Vaisitti, T.; Aydin, S.; Bergui, L.; D'Arena, G.; Bonello, L.; Omede, P.; Scatolini, M.; Jaksic, O.; Chiorino, G.; Efremov, D.; Malavasi, F., CD38 and ZAP-70 are functionally linked and mark CLL cells with high migratory potential. Blood, 2007, 110(12), 4012-4021.
66. Huttmann, A.; Klein-Hitpass, L.; Thomale, J.; Deenen, R.; Carpinteiro, A.; Nuckel, H.; Ebeling, P.; Fuhrer, A.; Edelmann, J.; Sellmann, L.; Duhrsen, U.; Durig, J., Gene expression signatures separate B-cell chronic lymphocytic leukaemia prognostic subgroups defined by ZAP-70 and CD38 expression status. Leukemia, 2006, 20(10), 1774-1782.
67. Pepper, C.; Brennan, P.; Alghazal, S.; Ward, R.; Pratt, G.; Starczynski, J.; Lin, T.; Rowntree, C.; Fegan, C., CD38+ chronic lymphocytic leukaemia cells co-express high levels of ZAP-70 and are functionally distinct from their CD38-counter-parts. Leukemia, 2006, 20(4), 743-744.
68. Zupo, S.; Isnardi, L.; Megna, M.; Massara, R.; Malavasi, F.; Dono, M.; Cosulich, E.; Ferrarini, M., CD38 expression distinguishes two groups of B-cell chronic lymphocytic leukemias with different responses to anti-IgM antibodies and propensity to apoptosis. Blood, 1996, 88(4), 1365-1374.
69. 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(3), 1087-1093.
70. Chen, L.; Widhopf, G.; Huynh, L.; Rassenti, L.; Rai, K. R.; Weiss, A.; Kipps, T. J., Expression of ZAP-70 is associated with increased B-cell receptor signaling in chronic lymphocytic leukemia. Blood, 2002, 100(13), 4609-4614.
71. Messmer, B. T.; Messmer, D.; Allen, S. L.; Kolitz, J. E.; Kudalkar, P.; Cesar, D.; Murphy, E. J.; Koduru, P.; Ferrarini, M.; Zupo, S.; Cutrona, G.; Damle, R. N.; Wasil, T.; Rai, K. R.; Hellerstein, M. K.; Chiorazzi, N., In vivo measurements document the dynamic cellular kinetics of chronic lymphocytic leukemia B cells. J. Clin. Invest., 2005, 115(3), 755-764.
72. Burger, J. A.; Ghia, P.; Rosenwald, A.; Caligaris-Cappio, F., The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood, 2009, 114(16), 3367-3375.
73. Deaglio, S.; Malavasi, F., Chronic lymphocytic leukemia microenvironment: shifting the balance from apoptosis to proliferation. Haematologica, 2009, 94(6), 752-756.
74. Deaglio, S.; Aydin, S.; Grand, M. M.; Vaisitti, T.; Bergui, L.; D'Arena, G.; Chiorino, G.; Malavasi, F., CD38/CD31 interactions activate genetic pathways leading to proliferation and migration in chronic lymphocytic leukemia cells. Mol. Med., 2010, 16(3-4), 87-91.
75. Lund, F. E., Signaling properties of CD38 in the mouse immune system: enzyme-dependent and-independent roles in immunity. Mol. Med., 2006, 12(11-12), 328-333.
76. Burger, J. A.; Kipps, T. J., CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood, 2006, 107(5), 1761-1767.
77. Deaglio, S.; Vaisitti, T.; Zucchetto, A.; Gattei, V.; Malavasi, F., CD38 as a molecular compass guiding topographical decisions of chronic lymphocytic leukemia cells. Semin. Cancer Biol., 2010, 20(6), 416-423.
78. Till, K. J.; Spiller, D. G.; Harris, R. J.; Chen, H.; Zuzel, M.; Cawley, J. C., CLL, but not normal, B cells are dependent on autocrine VEGF and alpha4beta1 integrin for chemokine-induced motility on and through endothelium. Blood, 2005, 105(12), 4813-4819.
79. Gattei, V.; Bulian, P.; Del Principe, M. I.; Zucchetto, A.; Maurillo, L.; Buccisano, F.; Bomben, R.; Dal-Bo, M.; Luciano, F.; Rossi, F. M.; Degan, M.; Amadori, S.; Del Poeta, G., Relevance of CD49d protein expression as overall survival and progressive disease prognosticator in chronic lymphocytic leukemia. Blood, 2008, 111(2), 865-873.
80. Shanafelt, T. D.; Geyer, S. M.; Bone, N. D.; Tschumper, R. C.; Witzig, T. E.; Nowakowski, G. S.; Zent, C. S.; Call, T. G.; Laplant, B.; Dewald, G. W.; Jelinek, D. F.; Kay, N. E., CD49d expression is an independent predictor of overall survival in patients with chronic lymphocytic leukaemia: a prognostic parameter with therapeutic potential. Br. J. Haematol., 2008, 140(5), 537-546.
81. Ley, K.; Laudanna, C.; Cybulsky, M. I.; Nourshargh, S., Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol., 2007, 7(9), 678-689.
82. Vaisitti, T.; Aydin, S.; Rossi, D.; Cottino, F.; Bergui, L.; D'Arena, G.; Bonello, L.; Horenstein, A. L.; Brennan, P.; Pepper, C.; Gaidano, G.; Malavasi, F.; Deaglio, S., CD38 increases CXCL12-mediated signals and homing of chronic lymphocytic leukemia cells. Leukemia, 2010, 24, 958-969.
83. Guo, W.; Giancotti, F. G., Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol., 2004, 5(10), 816-826.
84. Zucchetto, A.; Vaisitti, T.; Benedetti, D.; Tissino, E.; Bertagnolo, V.; Rossi, D.; Bomben, R.; Dal Bo, M.; Del Principe, M. I.; Gorgone, A.; Pozzato, G.; Gaidano, G.; Del Poeta, G.; Malavasi, F.; Deaglio, S.; Gattei, V., The CD49d/CD29 complex is physically and functionally associated with CD38 in B-cell chronic lymphocytic leukemia cells. Leukemia, 2012, 26(6), 1301-1312.
85. Zucchetto, A.; Benedetti, D.; Tripodo, C.; Bomben, R.; Dal Bo, M.; Marconi, D.; Bossi, F.; Lorenzon, D.; Degan, M.; Rossi, F. M.; Rossi, D.; Bulian, P.; Franco, V.; Del Poeta, G.; Deaglio, S.; Gaidano, G.; Tedesco, F.; Malavasi, F.; Gattei, V., 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(9), 4001-4009.
86. Bjorklund, M.; Koivunen, E., Gelatinase-mediated migration and invasion of cancer cells. Biochim. Biophys. Acta, 2005, 1755(1), 37-69.
87. Bauvois, B.; Dumont, J.; Mathiot, C.; Kolb, J. P., Production of matrix metalloproteinase-9 in early stage B-CLL: suppression by interferons. Leukemia, 2002, 16(5), 791-798.
88. Kamiguti, A. S.; Lee, E. S.; Till, K. J.; Harris, R. J.; Glenn, M. A.; Lin, K.; Chen, H. J.; Zuzel, M.; Cawley, J. C., The role of matrix metalloproteinase 9 in the pathogenesis of chronic lymphocytic leukaemia. Br. J. Haematol., 2004, 125(2), 128-140.
89. Redondo-Munoz, J.; Escobar-Diaz, E.; Samaniego, R.; Terol, M. J.; Garcia-Marco, J. A.; Garcia-Pardo, A., MMP-9 in B-cell chronic lymphocytic leukemia is up-regulated by alpha4beta1 integrin or CXCR4 engagement via distinct signaling pathways, localizes to podosomes, and is involved in cell invasion and migration. Blood, 2006, 108(9), 3143-3151.
90. Molica, S.; Vitelli, G.; Levato, D.; Giannarelli, D.; Vacca, A.; Cuneo, A.; Cavazzini, F.; Squillace, R.; Mirabelli, R.; Digiesi, G., Increased serum levels of matrix metalloproteinase-9 predict clinical outcome of patients with early B-cell chronic lymphocytic leukaemia. Eur. J. Haematol., 2003, 70(6), 373-378.
91. Vaisitti, T.; Serra, S.; Pepper, C.; Rossi, D.; Laurenti, L.; Gaidano, G.; Malavasi, F.; Deaglio, S., CD38 signals upregulate expression and functions of matrix metalloproteinase-9 in chronic lymphocytic leukemia cells. Leukemia, 2013, 27(5), 1177-1181.
92. Bichi, R.; Shinton, S. A.; Martin, E. S.; Koval, A.; Calin, G. A.; Cesari, R.; Russo, G.; Hardy, R. R.; Croce, C. M., Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc. Natl. Acad. Sci. U. S. A., 2002, 99(10), 6955-6960.
93. Johnson, A. J.; Lucas, D. M.; Muthusamy, N.; Smith, L. L.; Edwards, R. B.; De Lay, M. D.; Croce, C. M.; Grever, M. R.; Byrd, J. C., Characterization of the TCL-1 transgenic mouse as a preclinical drug development tool for human chronic lymphocytic leukemia. Blood, 2006, 108(4), 1334-1338.
94. Durig, J.; Ebeling, P.; Grabellus, F.; Sorg, U. R.; Mollmann, M.; Schutt, P.; Gothert, J.; Sellmann, L.; Seeber, S.; Flasshove, M.; Duhrsen, U.; Moritz, T., A novel nonobese diabetic/severe combined immunodeficient xenograft model for chronic lymphocytic leukemia reflects important clinical characteristics of the disease. Cancer Res., 2007, 67(18), 8653-8661.
95. Aydin, S.; Grabellus, F.; Eisele, L.; Mollmann, M.; Hanoun, M.; Ebeling, P.; Moritz, T.; Carpinteiro, A.; Nuckel, H.; Sak, A.; Gothert, J. R.; Duhrsen, U.; Durig, J., Investigating the role of CD38 and functionally related molecular risk factors in the CLL NOD/SCID xenograft model. Eur. J. Haematol., 2011, 87(1), 10-19.
96. Bagnara, D.; Kaufman, M. S.; Calissano, C.; Marsilio, S.; Patten, P.; Simone, R.; Chum, P.; Yan, X. J.; Allen, S. L.; Kolitz, J. E.; Baskar, S.; Rader, C.; Mellstedt, H.; Rabbani, H.; Lee, A.; Gregersen, P. K.; Rai, K. R.; Chiorazzi, N., A novel adoptive transfer model of chronic lymphocytic leukemia suggests a key role for T lymphocytes in the disease. Blood, 2011, 17(20), 5463-5472.
97. Wong, K. K.; Brenneman, F.; Chesney, A.; Spaner, D. E.; Gorczynski, R. M., Soluble CD200 is critical to engraft chronic lymphocytic leukemia cells in immunocompromised mice. Cancer Res., 2012, 72(19), 4931-4943.
98. Flemming, A., Deal watch: J&J and Genmab deal to push forward CD38 as a blood cancer target. Nat. Rev. Drug Discov., 2012, 11(11), 822.
99. Hersher, R., Companies wager high on CD38-targeting drugs for blood cancer. Nat. Med., 2012, 18(10), 1446.
100. de Weers, M.; Tai, Y. T.; van der Veer, M. S.; Bakker, J. M.; Vink, T.; Jacobs, D. C.; Oomen, L. A.; Peipp, M.; Valerius, T.; Slootstra, J. W.; Mutis, T.; Bleeker, W. K.; Anderson, K. C.; Lokhorst, H. M.; van de Winkel, J. G.; Parren, P. W., Daratumumab, a novel therapeutic human CD38 monoclonal antibody, induces killing of multiple myeloma and other hematological tumors. J. Immunol., 2011, 186(3), 1840-1848.
101. van der Veer, M. S.; de Weers, M.; van Kessel, B.; Bakker, J. M.; Wittebol, S.; Parren, P. W.; Lokhorst, H. M.; Mutis, T., The therapeutic human CD38 antibody daratumumab improves the antimyeloma effect of newly emerging multi-drug therapies. Blood Cancer J., 2011, 1(10), e41.
102. van der Veer, M. S.; de Weers, M.; van Kessel, B.; Bakker, J. M.; Wittebol, S.; Parren, P. W.; Lokhorst, H. M.; Mutis, T., Towards effective immunotherapy of myeloma: enhanced elimination of myeloma cells by combination of lenalidomide with the human CD38 monoclonal antibody daratumumab. Haematologica, 2011, 96(2), 284-290.
103. Deaglio, S.; Aydin, S.; Vaisitti, T.; Bergui, L.; Malavasi, F., CD38 at the junction between prognostic marker and therapeutic target. Trends Mol. Med., 2008, 14(5), 210-218.
104. Kellenberger, E.; Kuhn, I.; Schuber, F.; Muller-Steffner, H., Flavonoids as inhibitors of human CD38. Bioorg. Med. Chem. Lett., 2011, 21(13), 3939-3942.
105. Ross, J. A.; Kasum, C. M., Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr., 2002, 22, 19-34.
106. Escande, C.; Nin, V.; Price, N. L.; Capellini, V.; Gomes, A. P.; Barbosa, M. T.; O'Neil, L.; White, T. A.; Sinclair, D. A.; Chini, E. N., Flavonoid Apigenin Is an Inhibitor of the NAD+ase CD38: Implications for Cellular NAD+ Metabolism, Protein Acetylation, and Treatment of Metabolic Syndrome. Diabetes., 2013, 62(4), 1084-1093.
107. He, J.; Xu, Q.; Wang, M.; Li, C.; Qian, X.; Shi, Z.; Liu, L. Z.; Jiang, B. H., Oral Administration of Apigenin Inhibits Metastasis through AKT/P70S6K1/MMP-9 Pathway in Orthotopic Ovarian Tumor Model. Int. J. Mol. Sci., 2012, 13(6), 7271-7282.
108. Shukla, S.; Gupta, S., Molecular targets for apigenin-induced cell cycle arrest and apoptosis in prostate cancer cell xenograft. Mol. Cancer. Ther., 2006, 5(4), 843-852.
109. Shukla, S.; Mishra, A.; Fu, P.; MacLennan, G. T.; Resnick, M. I.; Gupta, S., Up-regulation of insulin-like growth factor binding protein-3 by apigenin leads to growth inhibition and apoptosis of 22Rv1 xenograft in athymic nude mice. FASEB J., 2005, 19(14), 2042-2044.