MCL1 transgenic mice exhibit a high incidence of B-cell lymphoma manifested as a spectrum of histologic subtypes

Blood

Volumn 97, Issue 12, 2001, Pages 3902-3909

  Zhou, Ping ^a,b,c   Levy, Norman B ^a,b,c   Xie, Haiyi ^a,b,c   Qian, Liping ^a,b,c   Lee, Chi Yu Gregory ^a,b,c   Gascoyne, Randy D ^a,b,c   Craig, Ruth W ^a,b,c  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; PROTEIN MCL 1;

ANIMAL MODEL; ARTICLE; B CELL LYMPHOMA; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL IMMORTALIZATION; CELL VIABILITY; FOLLICULAR LYMPHOMA; GENE EXPRESSION; LARGE CELL LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENE;

EID: 0035877981     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V97.12.3902     Document Type: Article

References (67)

1. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 1999;59(suppl):1693-1700.
2. Rudin CM, Thompson CB. Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu Rev Med. 1997;48:267-281.
3. Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with in vitro and in vivo chemoresponses. Blood. 1998;91:3379-3389.
4. Gascoyne RD, Adomat SA, Krajewski S, et al. Prognostic significance of Bcl-2 protein expression and Bcl-2 gene rearrangement in diffuse aggressive non-Hodgkin's lymphoma. Blood. 1997;90:244-251.
5. Ghia P, Boussiotis VA, Schultze JL, et al. Unbalanced expression of bcl-2 family proteins in follicular lymphoma: contribution of CD40 signaling in promoting survival. Blood. 1998;91:244-251.
6. Kaufmann SH, Karp JE, Svingen PA, et al. Elevated expression of the apoptotic regulator Mcl-1 at the time of leukemic relapse. Blood. 1998;91:991-1000.
7. Tsujimoto Y, Croce CC. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci U S A. 1986;83:5214-5218.
8. Rampino N, Yamamoto H, Ionov Y, et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science. 1997;275:967-969.
9. Meijerink JP, Mensink EJ, Wang K, et al. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood. 1998;91:2911-2997.
10. Knutsen T. Cytogenetic changes in the progression of lymphoma. Leuk Lymphoma. 1998;31:1-19.
11. Skarin AT, Dorfman DM. Non-Hodgkin's lymphomas: current classification and management. CA Cancer J Clin. 1997;47:351-372.
12. Limpens J, Stad R, Vos C, et al. Lymphoma-associated translocation t(14;18) in blood B cells of normal individuals. Blood. 1995;85:2528-2533.
13. Liu Y, Hernandez AM, Shibata D, Cortopassi GA. BCL2 translocation frequency rises with age in humans. Proc Natl Acad Sci U S A. 1994;91:8910-8914.
14. Corbally N, Grogan L, Keane MM, Devaney DM, Dervan PA, Carney DN. Bcl-2 rearrangement in Hodgkin's disease and reactive lymph nodes. Am J Clin Path. 1994;101:756-760.
15. Miret C, Font J, Molina R, et al. BCL-2 oncogene (B cell lymphoma/leukemia-2) levels correlate with systemic lupus erythematosus disease activity. Anticancer Res. 1999;19:3073-3076.
16. McDonnell TJ, Deane N, Platt FM, et al. bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 1989;57:79-88.
17. McDonnell TJ, Nunez G, Platt FM, et al. Deregulated Bcl-2-immunoglobulin transgene expands a resting but responsive immunoglobulin M and D-expressing B-cell population. Mol Cell Biol. 1990;10:1901-1907.
18. Strasser A, Harris AW, Cory S. Emu-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene. 1993;8:1-9.
19. Strasser A, Elefanty AG, Harris AW, Cory S. Progenitor tumours from Emu-bcl-2-myc transgenic mice have lymphomyeloid differentiation potential and reveal developmental differences in cell survival. EMBO J. 1996;15:3823-3834.
20. Cory S, Strasser A, Jacks T, et al. Enhanced cell survival and tumorigenesis. Cold Spring Harb Symp Quant Biol. 1995;59:365-375.
21. Cory S, Vaux DL, Strasser A, Harris AW, Adams JM. Insights from Bcl-2 and Myc: malignancy involves abrogation of apoptosis as well as sustained proliferation. Cancer Res. 1999;59 (suppl):1685-1692.
22. Strasser A, Whittingham S, Vaux DL, et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A. 1991;88:8661-8665.
23. Strasser A, Harris AW, Cory S. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell. 1991;67:889-899.
24. McDonnell TJ, Korsmeyer SJ. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14;18). Nature. 1991;349:254-256.
25. Pena JC, Rudin CM, Thompson CB. A Bcl-xL transgene promotes malignant conversion of chemically initiated skin papillomas. Cancer Res. 1998;58:2111-2116.
26. Harris AW, Strasser A, Bath ML, Elefanty AG, Cory S. Lymphomas and plasmacytomas in transgenic mice involving bcl2, myc and v-abl. Curr Top Microbiol Immunol. 1998;224:221-230.
27. Strasser A, Harris AW, Bath ML, Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature. 1990;348:331-333.
28. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Aced Sci U S A. 1993;90:3516-3520.
29. Yang T, Buchan HL, Townsend KJ, Craig RW. MCL-1, a member of the BCL-2 family, is induced rapidly in response to signals for cell differentiation or death, but not to signals for cell proliferation. J Cell Physiol. 1996;166:523-536.
30. Krajewski S, Bodrug S, Krajewska M, et al. Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am J Pathol. 1998;146:1309-1319.
31. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 2000;14:21-27.
32. Li L, Krajewski S, Reed JC, Choi YS. The apoptosis and proliferation of SAC-activated B cells by IL-10 are associated with changes in Bcl-2, Bcl-xL, and Mcl-1 expression. Cellular Immunol. 1997;178:33-41.
33. Moulding DA, Quayle JA, Hart CA, Edwards SW. Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood. 1998;92:2495-2502.
34. Chao JR, Wang JM, Lee SF, et al. Mcl-1 is an immediate-early gene activated by the granulocytemacrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol. 1998;18:4883-4898.
35. Lomo J, Blomhoff HK, Jacobsen SE, Krajewski S, Reed JC, Smeland EB. Interleukin-13 in combination with CD40 ligand potently inhibits apoptosis in human B lymphocytes: upregulation of Bcl-xL and Mcl-1. Blood. 1997;89:4415-4424.
36. Puthier D, Bataille R, Amiot M. IL-6 up-regulates mcl-1 in human myeloma cells through JAK/STAT rather than ras/MAP kinase pathway. Eur J Immunol. 1999;29:3945-3950.
37. Wang JM, Chao J-R, Chen W, Kuo M-L, Yen JJY, Yang-Yen HF. The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signaling pathway through a transcription factor complex containing CREB. Mol Cell Biol. 1999;19:6195-6206.
38. Townsend KJ, Trusty JL, Traupman MA, Eastman A, Craig RW. Expression of the antiapoptotic MCL1 gene product is regulated by a mitogen activated protein kinase-mediated pathway triggered through microtubule disruption and protein kinase C. Oncogene. 1998;17:1223-1234.
39. Townsend KJ, Zhou P, Bieszczad CK, Qian L, Craig RW. Regulation of MCL1 by a serum response factor/Elk-1-mediated mechanism links expression of a viability-promoting member of the Bcl-2 family to the induction of hematopoietic cell differentiation. J Biol Chem. 1999;274:1802-1813.
40. Lomo J, Smeland EB, Krajewski S, Reed JC, Blomhoff HK. Expression of the Bcl-2 homologue Mcl-1 correlates with survival of peripheral blood B lymphocytes. Cancer Res. 1996;56:40-43.
41. Altmeyer A, Simmons RC, Krajewski S, Reed JC, Bornkamm GW, Chen-Kiang S. Reversal of EBV immortalization precedes apoptosis in IL-6-induced human B cell terminal differentiation. Immunity. 1997;7:667-677.
42. Reynolds JE, Yang T, Qian L, et al. Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res. 1994;54:6348-6352.
43. Zhou P, Qian L, Kozopas KM, Craig RW. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood. 1997;89:630-643.
44. Zhou P, Qian L, Bieszczad CK, et al. Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types, allowing for immortalization in the myeloid lineage. Blood. 1998;92:3226-3239.
45. Hentunen TA, Jackson SH, Chung H, et al. Characterization of immortalized osteoclast precursors developed from mice transgenic for both bcl-XL and simian virus 40 large T antigen. Endocrinology. 1999;140:2954-2961.
46. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes hemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature. 1988;335:440-442.
47. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. Creation of human tumour cells with defined genetic elements. Nature. 1999;400:464-468.
48. Kozopas KM, Buchan HL, Craig RW. Improved coupling between proliferation-arrest and differentiation-induction in ML-1 human myeloblastic leukemia cells. J Cell Physiol. 1990;145:575-586.
49. Lee GCY, Wong E, Richter D, Menge AC. Monoclonal antibodies to human sperm antigens. J Reprod Immunol. 1984;6:227-238.
50. 2/M accumulation or protein phosphatase 1/2A inhibition. J Biol Chem. 2000;275:21686-21694.
51. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning, A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989:1.42-1.45.
52. Maki R, Roeder W, Traunecker A, et al. The role of DNA rearrangement and alternative RNA processing in the expression of immunoglobulin delta genes. Cell. 1981;24:353-365.
53. Feinberg AP, Vogelstein B. A technique for radio-labeling DNA fragments to high specific activity. Anal Biochem. 1983;132:6-13.
54. Murphy ED. Characteristic tumors. In Laboratory J, ed. Biology of the Laboratory Mouse. New York: Dover Publications; 1968:521-562.
55. Heston WE. Induction of mammary gland tumors in strain C57BL/He mice by isografts of hypophyses. J. Natl Cancer Inst. 1964;32:947-955.
56. Knowles DM, Cesarman E, Chadburn A, et al Correlative morphologic and molecular genetic analysis demonstrates three distinct categories of posttransplantation lymphoproliferative disorders. Blood. 1995;85:552-565.
57. Alizaheh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503-511.
58. Pattengale PK, Taylor CR. Experimental models of lymphoproliferative disease: the mouse as a model for human non-Hodgkin's lymphomas and related leukemias. Am J Pathol. 1983;113:237-265.
59. Tang JCO, Ho FCS, Chan ACL, Chow EYW, Srivastava G. Progression of spontaneous lymphomas in SJL mice: monitoring in vivo clonal evolution with molecular markers in sequential splenic samples. Lab Invest. 1998;78:1459-1466.
60. Yin CY, Knudson CM, Korsmeyer SJ, VanDyke T. Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature. 1997;385:637-640.
61. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, Raab-Traub N. Expression of the Epstein-Barr latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci U S A. 1998;95:11963-11968.
62. Sheppard RD, Samant SA, Rosenberg M, Silver L, Cole MD. Transgenic N-myc mouse model for indolent B cell lymphoma: tumor characterization and analysis of genetic alterations in spontaneous and retrovirally accelerated tumors. Oncogene. 1998;17:2073-2085.
63. Brown K, Balmain A. Transgenic mice and squamous multistage skin carcinogenesis. Cancer Metastasis Rev. 1995;14:113-124.
64. Ogilvy SS, Metcalf D, Grant CG, Bath ML, Harris AW, Adams JM. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc Natl Acad Sci U S A. 1999;96:14943-14948.
65. Traver D, Akashi K, Weissman I, Lagasse E. Mice defective in two apoptosis pathways in the myeloid lineage develop acute myeloblastic leukemia. Immunity. 1998;9:47-57.
66. Bingle CD, Craig RW, Hanks BM, Eaton V, Zhou P, Whyte MKB. Exon skipping in Mcl-1 results in a Bcl-2 homology domain 3 (BH3)-only gene product that promotes cell death. J Biol Chem. 2000;275:22136-22146.
67. Yang T, Kozopas KM, Craig RW. The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J Cell Biol. 1995;128:1173-1184.