Immunologic basis for the rare occurrence of true nonsecretory plasma cell dyscrasias

Journal of Leukocyte Biology

Volumn 76, Issue 3, 2004, Pages 528-536

  Decourt, Catherine ^a   Galea, Horia Radu ^a   Sirac, Christophe ^a   Cogné, Michel ^a,b  

^a DUPUYTREN UNIVERSITY HOSPITAL   (France)

^b CNRS   (France)

Author keywords

B cells; Immunoglobulin secretion; Immunoproliferative; Myeloma

Indexed keywords

IMMUNOGLOBULIN; IMMUNOGLOBULIN IDIOTYPE;

ADAPTATION; B LYMPHOCYTE; CELL CLONE; CELL CULTURE; CELL LINE; CELL LINEAGE; CLONAL ANERGY; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; IMMUNOLOGY; IMMUNOSURVEILLANCE; IN VIVO STUDY; LYMPHOCYTE; LYMPHOPROLIFERATIVE DISEASE; MOLECULAR MECHANICS; MUTATION; PLASMA CELL; PLASMA CELL DYSCRASIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; TRUE NONSECRETORY PLASMA CELL DYSCRASIA; TUMOR ESCAPE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; IMMUNOGLOBULINS; IMMUNOLOGIC SURVEILLANCE; MULTIPLE MYELOMA; PARAPROTEINEMIAS; PLASMA CELLS;

EID: 4344572134     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0803382     Document Type: Review

References (106)

1. Blair, A., Zahm, S. H. (1995) Agricultural exposures and cancer. Environ. Health Perspect. 103, Suppl 8, 205-208.
2. Massoudi, B. L., Talbott, E. O., Day, R. D., Swerdlow, S. H., Marsh, G. M., Kuller, L. H. (1997) A case-control study of hematopoietic and lymphoid neoplasms: the role of work in the chemical industry. Am. J. Ind. Med. 31, 21-27.
3. Gallagher, R. P., Threlfall, W. J. (1983) Cancer mortality in metal workers. Can. Med. Assoc. J. 129, 1191-1194.
4. Durie, B. G., Salmon, S. E. (1975) Cellular kinetics, staging and immunoglobulin synthesis in multiple myeloma. Anna. Rev. Med. 26, 283-288.
5. Warner, N. L., Potter, M., Metcalf, D. (1974) Multiple myeloma and related immunoglobulin-producing neoplasms. UICC Technical Rep. Ser. (N, L. Warner, Potter, M., Metcalf, D., eds.), vol. 13, I.
6. Bergsagel, D. E. (1972) Plasma cell myeloma. An interpretation review. Cancer 30, 1588-1594.
7. Caggiano, V., Cuttner, J., Solomon, A. (1967) Myeloma proteins, Bence Jones proteins and normal immunoglobulins in multiple myeloma. Blood 30, 265-287,
8. Cogné, M., Preud'homme, J. L. (1990) Gene deletions force nonsecretory αchain disease plasma cells to produce membrane-form α-chain only. J. Immunol. 145, 2455-2458.
9. Cogné, M., Guglielmi, P. (1993) Exon skipping without splice site mutation accounting for abnormal immunoglobulin chains in nonsecretory human myeloma. Eur. J. Immunol. 23, 1289-1293.
10. Aucouturier, P., Khamlichi, A. A., Preud'homme, J. L., Bauwens, M., Touchard, G., Cogné, M. (1992) Complementary DNA sequence of human amyloidogenic immunoglobulin light-chain prescursors. Biochem. J. 285, 149-152.
11. Aucouturier, P., Bauwens, M.. Khamlichi, A. A., Denoroy, L., Spinelli, S., Touchard, G., Preud'homme, J. L., Cogné, M. (1993) Monoclonal Ig L chain and L chain V domain fragment crystallization in myeloma-associated Fanconi's syndrome. J. Immunol. 150, 3561-3568.
12. I subgroup (ISE) in light chain deposition disease. Clin. Exp. Immunol. 91, 506-509.
13. III immunoglobulin light chain in myeloma with light chain deposition disease. Clin. Exp. Immunol. 106, 357-361.
14. Decourt, C., Touchard, G., Preud'homme, J. L., Vidai, R., Beaufils, H., Diemert, M. C., Cogné, M. (1998) Complete primary sequences of two λ light chains in myelomas with nonamyloid (Randall-type) light chain deposition disease. Am. J. Pathol. 153, 313-318.
15. Cogné, Galea, H. R., Siraa, C., Decourt, C. (2003) Immunoglobulin decreased solubility diseases: pathologies of the V domains? In Monoclonal Gammopathies and the Kidney. (Touchard, G., Aucouturier, P., Hermine, O., Ronco P. eds.), MA, Kluwer Academic Publishers, Dordrecht.
16. I, light chain responsible for incomplete proximal tubulopathy. Am. J. Kidney Dis. 41, 497-504.
17. Blade, J., Kyle, R. A. (1999) Nonsecretory myeloma, immunoglobulin D myeloma and plasma cell leukemia. Hematol. Oncol. Clin. North Am. 13, 1259-1272.
18. Mancilla, R., Davis, G. L. (1977) Nonsecretory multiple myeloma. Immunohistologic and ultrastructural observations on two patients. Am. J. Med. 63, 1015-1022.
19. Preud'homme, J. L., Hurez, D., Danon, F., Brouet, J. C., Seligmann, M. (1976) Intracytoplasmic and surface-bound immunoglobulins in "nonsecretory" and Bence Jones myeloma. Clin. Exp. Immunol. 25, 428-436.
20. IV subgroup in the kidney and plasma cells in light chain deposition disease. J. Clin. Invest. 87, 2186-2190.
21. Weiss, S., Lewinski, U. H., Pick, A. J., Gafter, U., Djaldetti, M. (1978) Ultrastructural features of the plasma cells in "non-secretory" myeloma. Blut 36, 149-157.
22. Border, W. A., Cohen, A. H. (1980) Renal biopsy diagnosis of clinically silent multiple myeloma. Ann. Intern. Med. 93, 43-46.
23. Drayson, M., Tang, L. X., Drew, R., Mead, G. P., Carr-Smith, H., Bradwell, A. R. (2001) Serum free light-chain measurements for identifying and monitoring patients with nonsecretory multiple myeloma. Blood 97, 2900-2902.
24. Weiss, S., Burrows, P. D., Meyer, J., Wabl, M. R. (1984) A Mott cell hybridoma. Eur. J. Immunol. 14, 744-748.
25. Weinstein, T., Mittelman, M., Djaldetti, M, (1987) Electron microscopy study of Mott and Russell bodies in myeloma cells. J. Submicrosc. Cytol. 19, 155-159.
26. Shultz, L. D., Coman, D. R., Lyons, B. L., Sidman, C. L., Taylor, S. (1987) Development of plasmacytoid cells with Russell bodies in autoimmune "viable motheaten" mice. Am. J. Pathol. 127, 38-50.
27. Schweitzer, P. A., Taylor, S. E., Shultz, L. D. (1991) Synthesis of abnormal immunoglobulins by hybridomas from autoimmune "viable motheaten" mutant mice. J. Cell Biol, 114, 35-43.
28. Valetti, C., Grossi, C. E., Milstein, C., Sitia. R. (1991) Russell bodies: a general response of secretory cells to synthesis of a mutant immunoglobulin which can neither exit from, nor be degraded in, the endoplasmic reticulum. J. Cell Biol 115, 983-994.
29. Cogné M., Silvain, C., Khamlichi, A. A., Preud'homme, J. L. (1992) Structurally abnormal immunoglobulins in human immunoproliferative disorders. Blood 79, 2181-2195.
30. Kohler, G., Potash, M. J., Lehrach, H., Schulman, M. J. (1982) Deletions in immunoglobulin μ chains. EMBO J. 1, 555-563.
31. Pepe, V. H., Sonenshein, G. E., Yoshimura, M. I., Shulman, M. J. (1986) Gene transfer of immunoglobulin light chain restores heavy chain secretion. J. Immunol. 137, 2367-2372.
32. Preud'homme, J. L., Brouet, J. C., Seligmann. M. (1979) Cellular immunoglobulins in human γ and α heavy chain diseases. Clin. Exp. Immunol. 37, 283-291.
33. Sonenshein, G. E., Siekevitz, M., Siebert, G. R., Gefter, M. L. (1978) Control of immunoglobulin secretion in the murine plasmacytoma line MOPC 315. J. Exp. Med. 148, 301-312.
34. Morrison, S. L., Scharff, M. D. (1979) A mouse myeloma variant with a defect in light chain synthesis. Eur. J. Immunol. 9, 461-465.
35. Kohler, G. (1980) Immunoglobulin chain loss in hybridoma lines. Proc. Natl. Acad. Sci. USA 77, 2197-2199.
36. Haas, I. G., Wabl, M. R. (1984) Immunoglobulin heavy chain toxicity in plasma cells is neutralized by fusion to pre-B cells. Proc. Natl. Acad. Sci. USA 81, 7185-7188.
37. Chou, C. L., Morrison, S. L. (1993) An insertion-deletion event in murine immunoglobulin κ gene resembles mutations at heavy-chain disease loci. Somat. Cell Mol. Genet. 19, 131-139.
38. Magrangeas, F., Cormier, M. L.. Descamps, G., Gouy, N., Lode, L., Mellerin, M. P., Harousseau, J. L., Bataille. R., Minvielle, S., Avet-Loiseau, H. (2004) Light-chain only multiple myeloma is due to the absence of functional (productive) rearrangement of the IgH gene at the DNA level. Blood 103, 3869-3875.
39. Goto, Y., Hamaguchi, K. (1982) Unfolding and refolding of the reduced constant fragment of the immunoglobulin light chain. Kinetic role of the intrachain disulfide bond. J. Mol. Biol. 156, 911-926.
40. Lilie, H., Buchner, J. (1995) Domain interactions stabilize the alternatively folded state of an antibody Fab fragment. FEBS Lett. 362, 43-46.
41. Amzel, L. M., Poljak, R. J. (1979) Three-dimensional structure of immunoglobulins. Annu. Rev. Biochem. 48, 961-997.
42. Kaloff, C. R., Haas, I. G. (1995) Coordination of immunoglobulin chain folding and immunoglobulin chain assembly is essential for the formation of functional IgG. Immunity 2, 629-637.
43. Haas. I. G., Wabl, M. (1983) Immunoglobulin heavy chain binding protein. Nature 306, 387-389.
44. Bole, D. G., Hendershot, L. M., Kearney, J. F. (1986) Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol. 102, 1558-1566.
45. Sommer, T., Wolf, D. H. (1997) Endoplasmic reticulum degradation: reverse protein flow of no return. FASEB J. 11, 1227-1233.
46. Brodsky, J. L., McCracken. A. A. (1997) ER-associated and proteasome-mediated protein degradation: how two topologically restricted events came together. Trends Cell Biol. 7, 151-156.
47. Wiertz, E, J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A., Ploegh. H. L. (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.
48. Alanen, A., Pira, U., Lassila, O., Roth, J., Franklin, R. M. (1985) Mott cells are plasma cells defective in immunoglohulin secretion. Eur. J. Immunol. 15, 235-242.
49. Reddy, P., Sparvoli, A., Fagioli: C., Fassina, G., Sitia, R. (1996) Formation of reversible disulfide bonds with the protein matrix of the endoplasmic reticulum correlates with the retention of unassembled Ig light chains. EMBO J. 15, 2077-2085.
50. Alanen, A., Pira, U., Colman, A., Franklin, R. M. (1987) Mott cells: a model to study immunoglobulin secretion. Eur. J. Immunol. 17, 1573-1577.
51. Lee, Y. K., Brewer, J. W., Hellman, R., Hendershot, L. M. (1999) BiP and immunoglobulin light chain cooperate to control the folding of heavy chain and ensure the fidelity of immunoglobulin assembly. Mol. Biol. Cell 10, 2209-2219.
52. Blond-Elguindi, S., Cwirla, S. E., Dower, W. J., Lipshutz, R. J., Sprang, S. R., Sambrook, J. F., Gething, M. J. (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75, 717-728.
53. Knarr, G., Gething, M. J., Modrow, S., Buchner, J. (1995) BiP binding sequences in antibodies. J. Biol. Chem. 270, 27589-27594.
54. Skowronek, M. H., Hendershot, L. M., Haas, I. G. (1998) The variable domain of nonassembled Ig light chain determines both the half-life and binding to the chaperone BiP. Proc. Natl. Acad. Sci. USA 95, 1574-1578.
55. Knittler, M. R., Dirks, S., Haas, I. G. (1995) Molecular chaperones involved in protein degradation in the endoplasmic reticulum: quantitative interaction of the heat shock cognate protein BiP with partially folded immunoglobulin light chains that are degraded in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92, 1764-1768.
56. Wei, L., Hendershot, L. M. (1995) Characterization of the nucleotide binding properties and ATPase activity of recombinant hamster BiP purified from bacteria. J. Biol. Chem. 270, 26670-26676.
57. Davis, D. P., Khurana, R., Meredith, S., Stevens, F. J., Argon, Y. (1999) Mapping the major interaction between binding protein and Ig light chains to sites within the variable domain. J. Immunol. 163, 3842-3850.
58. Cogné, M., Aucouturier, P., Brizard, A., Dreyfus, B., Duarte, F.. Preud'homme, J. L. (1993) Complete variable region deletion in a μ heavy chain disease protein (ROUL). Correlation with light chain secreuon. Leuk. Res. 17, 527-532.
59. Cogné, M., Mounir, S., Mahdi, T., Preud'homme, J. L., Nau, F., Guglielmi, P. (1990) Production of an abnormal μ chain with a shortened VHIV subgroup variable region in a Burkitt's lymphoma cell line. Mol. Immunol. 27, 929-934.
60. Mounir, S., Guglielmi, P., Preud'homme, J. L., Nau, F., Cogné, M. (1990) Alternate splice sites within the human VH gene coding sequences lead to truncated Ig mu-chains. J. Immunol. 144, 342-347.
61. Cogné, M., Mounir, S., Preud'homme, J. L., Nau, F., Guglielmi, P. (1988) Burkitt's lymphoma cell lines producing truncated μ immunoglobulin heavy chains lacking part of the variable region. Eur. J. Immunol. 18, 1485-1489.
62. Bakhshi, A., Guglielmi, P., Siebenlist, U., Ravetch, J. V., Jensen, J. P., Korsmeyer, S. J. (1986) A DNA insertion/deletion necessitates an aberrant RNA splice accounting for a μ heavy chain disease protein. Proc. Natl. Acad. Sci. USA 83, 2689-2693.
63. Hendershot, L. M., Bole, D., Kohler, G., Kearney, J. F. (1987) Assembly and secretion of heavy chains that do not associate postranslationally with immunoglobulin heavy chain-binding protein. J. Cell Biol. 104, 761-767.
64. Ho, S. C., Chaudhuri, S., Bachhawat, A., McDonald, K., Pillai, S. (2000) Accelerated proteasomal degradation of membrane Ig heavy chains. J. Immunol. 164, 4713-4719.
65. Mosmann, T. R., Williamson, A. R. (1980) Structural mutations in a mouse immunoglobulin light chain resulting in failure to be secreted. Cell 20, 283-292.
66. Morrison, S. L., Seharff, M. D. (1975) Heavy chain-producing variants of a mouse myeloma cell line. J. Immunol. 114, 655-659.
67. Leitzgen, K., Knittler, M. R., Haas, I. G. (1997) Assembly of immunoglobulin light chains as a prerequisite for secretion. J. Biol. Chem. 272, 3117-3123.
68. Ma, J., Kearney, J. F., Hendershot, L. M. (1990) Association of transport-defective light chains with immunoglobulin heavy chain binding protein. Mol. Immunol. 27, 623-630.
69. Dul, J. L., Argon, Y. (1990) A single amino acid substitution in the variable region of the light chain specifically blocks immunoglobulin secretion. Proc. Natl. Acad. Sci. USA 87, 8135-8139.
70. Dul, J. L., Aviel, S., Melnick, J., Argon, Y. (1996) Ig light chains are secreted predominantly as monomers. J. Immunol. 157, 2969-2975.
71. Kuehl, W. M., Seharff, M. D. (1974) Synthesis of a carboxyl-terminal (constant region) fragment of the immunoglobulin light chain by a mouse myeloma cell line. J. Mol. Biol. 89, 409-421.
72. Wu, G. E., Hozumi, N., Murialdo, H. (1983) Secretion of a λ 2 immunoglobulin chain is prevented by a single amino acid substitution in its variable region. Cell 33, 77-83.
73. Jack, H. M., Sloan, B., Grisham, G., Reason, D., Wabl, M. (1993) Large cytoplasmic inclusion body κ-chain has unusual intrachain disulfide bonding. J. Immunol. 150, 4928-4933.
74. Khamliehi, A. A., Rocca, A., Touchard, G., Aucouturier, P., Preud'homme, J. L., Cogné, M. (1995) Role of light chain variable region in myeloma with light chain deposition disease: evidence from an experimental model. Blood 86, 3655-3659.
75. Decourt, C., Rocca, A., Bridoux, F., Vrtovsnik, F., Preud'homme, J. L., Cogné, M., Touchard, G. (1999) Mutational analysis in murine models for myeloma associated Fanconi's syndrome or cast myeloma nephropathy. Blood 94, 3559-3566.
76. Chauveau, C., Decourt, C., Cogné, M. (1998) Insertion of the IgH locus 3′ regulatory palindrome in expression vectors warrants sure and efficient expression in stable B cell transfectants. Gene 222, 279-285.
77. Jack, H. M., Beck-Engeser, G., Sloan, B., Wong, M. L., Wabl, M. (1992) A different sort of Mott cell. Proc. Nad. Acad. Sci. USA 89, 11688-11691.
78. Dul, J. L., Burrone, O. R., Argon, Y. (1992) A conditional secretory mutant in an IgL chain is caused by replacement of tyrosine/phenylalanine 87 with histidine. J. Immunol. 149, 1927-1933.
79. Gass, J. N., Gifford, N. M., Brewer, J. W. (2002) Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J. Biol. Chem. 277, 49047-49054.
80. Lin, K. L, Tunyaplin, C., Calame, K. (2003) Transcriptional regulatory cascades controlling plasma cell differentiation. Immunol. Rev. 194, 19-28.
81. Iwakoshi, N. N., Lee, A. H., Glimcher, L. H. (2003) The X-box bonding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response. Immunol. Rev. 194, 29-38.
82. Calame, K. L., Lin, K. L, Tunyaplin, C. (2003) Regulatory mechanisms that determine the development and function of plasma cells. Anna. Rev. Immunol. 21, 205-230.
83. Shaffer, A. L., Lin, K. I., Kuo, T. C., Yu, X., Hurt, E. M., Rosenwald, A., Giltnane, J. M., Yang, L., Zhao, H., Calame, K., Staudt, L. M. (2002) Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program, Immunity 17, 51-62.
84. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G., Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
85. Couture, M. L., Heath, C. A. (1995) Relationship between loss of heavy chains and the appearance of nonproducing hybridomas. Biotechnol. Bioeng. 47, 270-275.
86. Kromenaker, S. J., Srienc, F. (1994) Stability of producer hybridoma cell lines after cell sorting: a case study. Biotechnol. Prog. 10, 299-307.
87. Ozturk, S. S., Palsson, B. O. (1990) Loss of antibody productivity during long-term cultivation of a hybridoma cell line in low serum and serum-free media. Hybridoma 9, 167-175.
88. Wu, H. Y., Kaartinen, M. (1995) The somatic hypermutation activity of a follicular lymphoma links to large insertions and deletions of immunoglobulin genes. Scand. J. Immunol. 42, 52-59.
89. Weiss, S., Wu, G. E. (1987) Somatic point mutations in unrearranged immunoglobulin gene segments encoding the variable region of λ light chains. EMBO J. 6, 927-932.
90. Denepoux, S., Razanajaona, D., Blanchard, D., Meffre, G., Capra, J. D., Banchereau, J., Lebecque, S. (1997) Induction of somatic mutation in a human B cell line in vitro. Immunity 6, 35-46.
91. Rengers, J. U., Touchard, G., Decourt, C., Déret, S., Michel, H., Cogné, M. (2000) Importance of heavy and light chain primary strucutres for IgG3 nephritogenicity in an experimental model for cryocrystalglobulinemia. Blood 95, 3467-3472.
92. Van Endert, P. M. (1999) Genes regulating MHC class I processing of antigen. Curr. Opin. Immunol. 11, 82-88.
93. Groettrup, M., Soza, A., Kuckelkorn, U., Kloetzel, P. M. (1996) Proteasome activity limits the assembly of MHC class I molecules after IFN-γ stimulation. Immunol. Today 17, 429-435.
94. Momburg, F., Hammerling, H. G. (1998) Generation and TAP-mediated transport of peptides for major histocompatibility complex class I molecules. Adv. Immunol. 68, 191-256.
95. Sadasivan, B., Lehner, P. J., Ortmann, B., Spies, T., Cresswell, P. (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5, 103-114.
96. Chakrabarti, D., Ghosh, S. K. (1992) Induction of syngeneic cytotoxic T lymphocytes against a B cell tumor. I. Role of idiotypic immunoglobulin. Cell. Immunol. 142, 54-66.
97. Chakrabarti, D., Ghosh, S. K. (1992) Induction of syngeneic cytotoxic T lymphocytes against a B cell tumor. II. Characterization of anti-idiotypic CTL lines and clones. Cell. Immunol. 144, 443-454.
98. Halapi, E., Werner, A, Wahlstrom, J., Osterborg, A., Jeddi-Tehrani, M., Yi, Q., Janson, C. H., Wigzell, H., Grunewald, J., Mellstedt, H. (1997) T cell repertoire in patients with multiple myeloma and monoclonal gammopathy of undetermined significance: clonal CD8+ T cell expansions are found preferentially in patients with a low tumor burden. Eur. J. Immumol. 27, 2245-2252.
99. Galea, H. R., Cogné, M. (2002) GM-CSF and IL-12 production by malignant plasma cells promotes cell-mediated immune responses against monoclonal Ig determinants in a light chain myeloma model. Clin. Exp. Immunol. 129, 247-253.
100. Galea, H. R., Denizot, Y., Cogné, M. (2002) Light chain myeloma plasma cells induce a strong cell-mediated immune response mainly directed against the monoclonal light chain determinants in a murine experimental model. Cancer Immunol. Immunother. 51, 229-234.
101. Messiaen, T., Déret, S., Mougenot, B., Bridoux, F., Dequiedt, P., Dion, J. J., Makdassi, R., Meeus, F., Pourrai, J., Touchard, G., Vanhille, P., Zaoui, P., Aucouturier, P., Ronco, P. M. (2000) Adult Fanconi syndrome secondary to light chain gammopathy. Clinicopathologic heterogeneity and unusual features in 11 patients. Medicine (Baltimore) 79, 135-154.
102. Maldonado, J. E., Velosa, J. A., Kyle, R. A., Wagoner, R. D., Holley, K. E., Salassa, R. M. (1975) Fanconi syndrome in adults: a manifestation of a latent form of myeloma. Am. J. Med. 58, 354-364.
103. Bogen, B., Schenck, K., Munthe, L. A., Denibic, Z. (2000) Deletion of idiotype (Id)-specific T cells in multiple myeloma. Acta Oncol. 39, 783-788.
104. Smith, D. B., Harris, M., Gowland, E., Chang, J., Scarffe, J. H. (1986) Non-secretory multiple myeloma: a report of 13 cases with a review of the literature. Hematol. Oncol. 4, 307-313.
105. Lam, K. P., Kuhn, R., Rajewsky, K. (1997) In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90, 1073-1083.
106. Reth, M., Wienands, J., Schamel, W. W. (2000) An unsolved problem of the clonal selection theory and the model of an oligomeric B-cell antigen receptor. Immunol. Rev. 176, 10-11.