Home LiteratureArticle Details
PMID: 11805288 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

IL-6 transgenic mouse model for extraosseous plasmacytoma.

Kovalchuk AL, Kim JS, Park SS, Coleman AE, Ward JM, Morse HC, Kishimoto T, Potter M, Janz S

Abstract

Plasma cell neoplasms in humans comprise plasma cell myeloma, otherwise known as multiple myeloma, Ig deposition and heavy chain diseases, and plasmacytoma (PCT). A subset of PCT, designated extramedullary PCT, is distinguished from multiple myeloma and solitary PCT of bone by its distribution among various tissue sites but not the bone marrow. Extramedullary (extraosseus) PCT are rare spontaneous neoplasms of mice but are readily induced in a susceptible strain, BALB/c, by treatment with pristane. The tumors develop in peritoneal granulomas and are characterized by Myc-activating T(12;15) chromosomal translocations and, most frequently, by secretion of IgA. A uniting feature of human and mouse plasma cell neoplasms is the critical role played by IL-6, a B cell growth, differentiation, and survival factor. To directly test the contribution of IL-6 to PCT development, we generated BALB/c mice carrying a widely expressed IL-6 transgene. All mice exhibited lymphoproliferation and plasmacytosis. By 18 months of age, over half developed readily transplantable PCT in lymph nodes, Peyer's patches, and sometimes spleen. These neoplasms also had T(12;15) translocations, but remarkably, none expressed IgA. Unexpectedly, approximately 30% of the mice developed follicular and diffuse large cell B cell lymphomas that often coexisted with PCT. These findings provide a unique model of extramedullary PCT for studies on pathogenesis and treatment and suggest a previously unappreciated role for IL-6 in the genesis of germinal center-derived lymphomas.

MeSH Terms
Animals Cell Differentiation Cell Division Cell Survival Chromosome Mapping Disease Models, Animal Genes, myc Granuloma/immunology Humans In Situ Hybridization, Fluorescence Interleukin-6/genetics,immunology Lymphoma, B-Cell/immunology,pathology Mice Mice, Inbred C57BL Mice, Transgenic Neoplasm Transplantation/immunology Plasmacytoma/genetics,immunology,pathology Time Factors Translocation, Genetic
Chemicals
Interleukin-6
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Kovalchuk Alexander L
Laboratory of Genetics, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Kim Joong Su
Park Sung Sup
Coleman Allen E
Ward Jerrold M
Morse Herbert C
Kishimoto Tadamitsu
Potter Michael
Janz Siegfried
References (43)
43 references, click to expand
  1. Development of progressive kidney damage and myeloma kidney in interleukin-6 transgenic mice.
    Blood. 1994 May 1;83(9):2570-9 PMID: 7513204
  2. Identification of two genes on chromosome 4 that determine resistance to plasmacytoma induction in mice.
    Cancer Res. 1994 Feb 15;54(4):969-75 PMID: 8313388
  3. Differences in the molecular structure of c-myc-activating recombinations in murine plasmacytomas and precursor cells.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12066-70 PMID: 7991585
  4. An interleukin-6 transgene expressed in B lymphocyte lineage cells overcomes the T cell-dependent establishment of normal levels of switched immunoglobulin isotypes.
    Eur J Immunol. 1995 May;25(5):1332-7 PMID: 7774636
  5. Interleukin 6 is essential for in vivo development of B lineage neoplasms.
    J Exp Med. 1995 Jul 1;182(1):243-8 PMID: 7790819
  6. Differences between Burkitt's lymphomas and mouse plasmacytomas in the immunoglobulin heavy chain/c-myc recombinations that occur in their chromosomal translocations.
    Cancer Res. 1995 Nov 1;55(21):5012-8 PMID: 7585544
  7. Elevated interleukin 6 is induced by prostaglandin E2 in a murine model of inflammation: possible role of cyclooxygenase-2.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4885-90 PMID: 8643498
  8. IL-6 expression in neurons of transgenic mice causes reactive astrocytosis and increase in ramified microglial cells but no neuronal damage.
    Eur J Neurosci. 1995 Dec 1;7(12):2441-9 PMID: 8845949
  9. Distinct tumorigenic potential of abl and raf in B cell neoplasia: abl activates the IL-6 signaling pathway.
    Immunity. 1996 Jul;5(1):81-9 PMID: 8758897
  10. Defective development of pristane-oil-induced plasmacytomas in interleukin-6-deficient BALB/c mice.
    Am J Pathol. 1997 Sep;151(3):689-96 PMID: 9284817
  11. Deletional remodeling of c-myc-deregulating chromosomal translocations.
    Oncogene. 1997 Nov 6;15(19):2369-77 PMID: 9393881
  12. Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13130-4 PMID: 9789053
  13. Accelerated apoptosis of lymphocytes by augmented induction of Bax in SSI-1 (STAT-induced STAT inhibitor-1) deficient mice.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15577-82 PMID: 9861011
  14. STAT3 is required for the gp130-mediated full activation of the c-myc gene.
    J Exp Med. 1999 Jan 4;189(1):63-73 PMID: 9874564
  15. BALB/c.CBA/N mice carrying the defective Btk(xid) gene are resistant to pristane-induced plasmacytomagenesis.
    Int Immunol. 1999 Jul;11(7):1059-64 PMID: 10383938
  16. Negative regulation of cytokine signaling: STAT-induced STAT inhibitor.
    Trends Biochem Sci. 1999 Oct;24(10):394-8 PMID: 10500304
  17. Diverse karyotypic abnormalities of the c-myc locus associated with c-myc dysregulation and tumor progression in multiple myeloma.
    Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):228-33 PMID: 10618400
  18. Accelerated appearance of multiple B cell lymphoma types in NFS/N mice congenic for ecotropic murine leukemia viruses.
    Lab Invest. 2000 Feb;80(2):159-69 PMID: 10701686
  19. Clonal diversification of primary BALB/c plasmacytomas harboring T(12;15) chromosomal translocations.
    Leukemia. 2000 May;14(5):909-21 PMID: 10803525
  20. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors.
    Oncogene. 2000 May 15;19(21):2548-56 PMID: 10851053
  21. Lymph nodes and Peyer's patches of IL-6 transgenic BALB/c mice harbor T(12;15) translocated plasma cells that contain illegitimate exchanges between the immunoglobulin heavy-chain mu locus and c-myc.
    Leukemia. 2000 Jun;14(6):1127-35 PMID: 10865979
  22. Constitutive activation of STAT3 is associated with the acquisition of an interleukin 6-independent phenotype by murine plasmacytomas and hybridomas.
    Blood. 2000 Nov 15;96(10):3514-21 PMID: 11071649
  23. Efficiency alleles of the Pctr1 modifier locus for plasmacytoma susceptibility.
    Mol Cell Biol. 2001 Jan;21(1):310-8 PMID: 11113205
  24. The role of interleukin-6 and interleukin-6/interleukin-6 receptor-alpha complex in the pathogenesis of multiple myeloma.
    Eur Cytokine Netw. 2000 Dec;11(4):546-51 PMID: 11125296
  25. Combined histologic and molecular features reveal previously unappreciated subsets of lymphoma in AKXD recombinant inbred mice.
    Leuk Res. 2001 Aug;25(8):719-33 PMID: 11397479
  26. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria.
    Nature. 2001 Oct 11;413(6856):639-43 PMID: 11675788
  27. Genetics of susceptibility to plasmacytoma induction. I. BALB/cAnN (C), C57BL/6N (B6), C57BL/Ka (BK), (C times B6)F1, (C times BK)F1, and C times B recombinant-inbred strains.
    J Natl Cancer Inst. 1975 Jun;54(6):1413-7 PMID: 1133851
  28. A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro.
    Science. 1986 Aug 1;233(4763):566-9 PMID: 3726549
  29. Activation of cellular oncogenes in hemopoietic cells by chromosome translocation.
    Adv Cancer Res. 1986;47:189-234 PMID: 3096089
  30. Activation of the c-myc oncogene in a precursor-B-cell blast crisis of follicular lymphoma, presenting as composite lymphoma.
    N Engl J Med. 1988 May 26;318(21):1373-8 PMID: 3285208
  31. IgG1 plasmacytosis in interleukin 6 transgenic mice.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7547-51 PMID: 2798426
  32. Interleukin 6 induces secretion of IgG1 by coordinated transcriptional activation and differential mRNA accumulation.
    Proc Natl Acad Sci U S A. 1989 Oct;86(20):8024-8 PMID: 2813375
  33. Mouse plasmacytoma growth in vivo: enhancement by interleukin 6 (IL-6) and inhibition by antibodies directed against IL-6 or its receptor.
    J Exp Med. 1990 Sep 1;172(3):997-1000 PMID: 2388041
  34. Generation of plasmacytomas with the chromosomal translocation t(12;15) in interleukin 6 transgenic mice.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):232-5 PMID: 1729694
  35. A retrovirus that expresses v-abl and c-myc oncogenes rapidly induces plasmacytomas.
    Oncogene. 1992 Apr;7(4):811-9 PMID: 1565479
  36. Interleukin 6: insights to its function in skin by overexpression in transgenic mice.
    Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5068-72 PMID: 1375756
  37. MYC rearrangements in histologically progressed follicular lymphomas.
    Blood. 1992 Aug 1;80(3):758-67 PMID: 1638027
  38. Long-term consequences of interleukin-6 overexpression in transgenic mice.
    DNA Cell Biol. 1992 Oct;11(8):587-92 PMID: 1382446
  39. Plasmacytomagenesis in mice: model of neoplastic development dependent upon chromosomal translocations.
    Carcinogenesis. 1992 Oct;13(10):1681-97 PMID: 1423827
  40. In vitro culture of primary plasmacytomas requires stromal cell feeder layers.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2060-4 PMID: 8446628
  41. Detection of recombinations between c-myc and immunoglobulin switch alpha in murine plasma cell tumors and preneoplastic lesions by polymerase chain reaction.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7361-5 PMID: 8346257
  42. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10061-5 PMID: 7694279
  43. Airway epithelial cell expression of interleukin-6 in transgenic mice. Uncoupling of airway inflammation and bronchial hyperreactivity.
    J Clin Invest. 1994 Nov;94(5):2028-35 PMID: 7962549
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-02-05
Epub
2002-00-22
Pages
1509-14
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC122221
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com