Impaired B lymphopoiesis in old age: A role for inflammatory B cells?

Immunologic Research

Volumn 57, Issue 1-3, 2013, Pages 361-369

  Riley, Richard L ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Age associated B cells; Aging; B lymphopoiesis; Inflammation

Indexed keywords

PRE B CELL RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; BONE MARROW CELL; CELL SHAPE; CELL SPECIFICITY; DEGRADATION; FEEDBACK SYSTEM; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNITY; LYMPHOCYTE DEPLETION; LYMPHOPOIESIS; MICROENVIRONMENT; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SENESCENCE;

AGE FACTORS; AGING; ANIMALS; B-LYMPHOCYTES; CELLULAR MICROENVIRONMENT; HUMANS; IMMUNOMODULATION; INFLAMMATION; LYMPHOPOIESIS;

EID: 84891496727     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-013-8444-5     Document Type: Article

References (71)

1. Linton PJ, Dorshkind K. Age-related changes in lymphocyte development and function. Nat Immunol. 2004;5:133-9.
2. Cancro M, Hao Y, Scholz J, Riley R, Frasca D, Dunn-Walters D, Blomberg BB. B cells and aging: molecules and mechanisms. Trends Immunol. 2009;30:313-8.
3. Scholz JL, Diaz A, Riley RL, Cancro MP, Frasca D. A comparative review of aging and B cell function in mice and humans. Curr Opin Immunol. 2013;25:504-10.
4. Miller JP, Cancro MP. B cells and aging: balancing the homeostatic equation. Exp Gerontol. 2007;42:396-9.
5. Vasto S, Candore G, Balistreri CR, Caruso M, Colonna-Romano G, Grimaldi MP, Listi F, Nuzzo D, Lio D, Caruso C. Inflammatory networks in ageing, age-related diseases and longevity. Mech Ageing Dev. 2007;128:83-91.
6. Hao Y, O'Neill P, Naradikian M, Scholz J, Cancro MP. A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood. 2011;118:1294-304.
7. Rubtsov A, Rubtsova K, Fischer A, Meehan R, Gillis J, Kappler J, Marrack P. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c(+) B-cell population is important for the development of autoimmunity. Blood. 2011;118:1305-15.
8. Ratliff M, Alter S, Frasca D, Blomberg BB, Riley RL. In senescence, age-associated B cells secrete TNFα and inhibit survival of B-cell precursors. Aging Cell. 2013;12:177-332.
9. Riley RL, Kruger MG, Elia J. B cell precursors are decreased in senescent BALB/c mice, but retain normal mitotic activity in vivo and in vitro. Clin Immunol Immunopathol. 1991;59:301-13.
10. Stephan RP, Sanders VM, Witte PL. Stage-specific alterations in murine B lymphopoiesis with age. Int Immunol. 1996;8:509-18.
11. Van der Put E, Sherwood EM, Blomberg BB, Riley RL. Aged mice exhibit distinct B cell precursor phenotypes differing in activation, proliferation and apoptosis. Exp Gerontol. 2003;38:1137-47.
12. Labrie JE, Sah A, Allman D, Cancro M, Gerstein R. Bone marrow microenvironmental changes underlie reduced RAG-mediated recombination and B cell generation in aged mice. J Exp Med. 2004;200:411-23.
13. Melchers F, ten Boekel E, Seidl T, Kong XC, Yamagami T, Onishi K, Shimizu T, Rolink AG, Andersson J. Repertoire selection by pre-B-cell receptors and B-cell receptors, and genetic control of B-cell development from immature to mature B cells. Immunol Rev. 2000;175:33-46.
14. Sherwood E, Blomberg BB, Xu W, Warner C, Riley R. Senescent BALB/c mice exhibit decreased expression of lambda5 surrogate light chains and reduced development within the pre-B cell compartment. J Immunol. 1998;161:4472-5.
15. Sherwood E, Xu W, King A, Blomberg BB, Riley RL the reduced expression of surrogate light chains in B cell precursors from senescent BALB/c mice is associated with decreased E2A proteins. Mech Ageing Dev. 2000;118:45-59.
16. Kirman I, Zhao K, Wang Y, Szabo P, Telford W, Weksler ME. Increased apoptosis of bone marrow pre-B cells in old mice associated with their low number. Int Immunol. 1998;10:1385-92.
17. Johnson KM, Owen K, Witte PL. Aging and developmental transitions in the B cel lineage. Int Immunol. 2002;14:1313-23.
18. Shahaf G, Johnson K, Mehr R. B cell development in aging mice: lessons from mathematical modeling. Int Immunol. 2006;18:31-9.
19. Rossi MI, Yokota T, Medina KL, Garrett KP, Comp PC, Schipul AH Jr, Kincade PW. B lymphopoiesis is active throughout human life, but there are developmental age-related changes. Blood. 2003;101:576-84.
20. Nunez C, Nishimoto N, Gartland GL, Billips LG, Burrows PD, Kubagawa H, Cooper MD. B cells are generated throughout life in humans. J Immunol. 1996;156:866-72.
21. McKenna RW, Washington LT, Aquino DB, Picker LJ, Kroft SH. Immunophenotypic analysis of hematogones (B-lymphocyte precursors) in 662 consecutive bone marrow specimens by 4-color flow cytometry. Blood. 2001;98:2498-507.
22. Muller-Sieburg CE, Sieburg HB, Bernitz JM, Cattarossi G. Stem cell heterogeneity: implications for aging and regenerative medicine. Blood. 2012;119:3900-7.
23. Shimazu T, Iida R, Zhang Q, Welner RS, Medina KL, Alberola-Lla J, Kincade PW. CD86 is expressed on murine hematopoietic stem cells and denotes lymphopoietic potential. Blood. 2012;119:4889-97.
24. Esplin BL, Shimazu T, Welner RS, Garrett KP, Nie L, Zhang Q, Humphrey MB, Yang Q, Borghesi LA, Kincade PW. Chronic exposure to a TLR ligand injures hematopoietic stem cells. J Immunol. 2011;186:5367-75.
25. Miller J, Allman D the decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J Immunol. 2003;171:2326-30.
26. Lescale C, Dias S, Maes J, Cumano A, Szabo P, Charron D, Weksler ME, Dosquet C, Vieira P, Goodhardt M. Reduced EBF expression underlies loss of B-cell potential of hematopoietic progenitors with age. Aging Cell. 2010;9:410-9.
27. Frasca D, Nguyen D, Riley RL, Blomberg BB. Decreased E12 and/or E47 transcription factor activity in the bone marrow as well as in the spleen of aged mice. J Immunol. 2003;170:719-26.
28. Van der Put E, Frasca D, King AM, Blomberg BB, Riley RL. Decreased E47 in senescent B cell precursors is stage specific and regulated posttranslationally by protein turnover. J Immunol. 2004;173:818-27.
29. King AM, Van der Put E, Blomberg BB, Riley RL. Accelerated Notch-dependent degradation of E47 proteins in aged B cell precursors is associated with increased ERK MAPK activation. J Immunol. 2007;178:3521-9.
30. Sigvardsson M, O'Riordan M, Grosschedl R. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity. 1997;7:25-36.
31. Medina KL, Singh H. Genetic networks that regulate B lymphopoiesis. Curr Opin Hematol. 2005;12:203-9.
32. Rolink AG, Schaniel C, Busslinger M, Nutt SL, Melchers F. Fidelity and infidelity in commitment to B-lymphocyte lineage development. Immunol Rev. 2000;175:104-11.
33. Schebesta M, Pfeffer PL, Busslinger M. Control of pre-BCR signaling by Pax5-dependent activation of the BLNK gene. Immunity. 2002;17:473-85.
34. Siegel R, Kim U, Patke A, Yu X, Ren X, Tarakhovsky A, Roeder RG. Nontranscriptional regulation of SYK by the coactivator OCA-B is required at multiple stages of B cell development. Cell. 2006;125:761-74.
35. Zandi S, Mansson R, Tsapogas P, Zetterblad J, Bryder D, Sigvardsson M. EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors. J Immunol. 2008;181:3364-72.
36. Yasuda T, Hayakawa F, Kurahashi S, Sugimoto K, Minami Y, Tomita A, Naoe T. B cell receptor-ERK1/2 signal cancels PAX5-dependent repression of BLIMP1 through PAX5 phosphorylation: a mechanism of antigen-triggering plasma cell differentiation. J Immunol. 2012;188:6127-34.
37. Zwilling S, Dieckmann A, Pfisterer P, Angel P, Wirth T. Inducible expression and phosphorylation of coactivator BOB.1/OBF.1 in T cells. Science. 1997;277:221-5.
38. Stephan RP, Reilly CR, Witte PL. Impaired ability of bone marrow stromal cells to support B-lymphopoiesis with age. Blood. 1998;91:75-88.
39. Stephan RP, Lill-Elghanian DA, Witte PL. Development of B cells in aged mice: decline in the ability of pro-B cells to respond to IL-7 but not to other growth factors. J Immunol. 1997;158:1598-609.
40. Ergen AV, Boles NC, Goodel MA. Rantes/Ccl5 influences hematopoietic stem cell subtypes and causes myeloid skewing. Blood. 2012;119:2500-9.
41. Su DM, Aw D, Palmer DB. Immunosenescence: a product of the environment? Curr Opin Immunol. 2013;25:498-503.
42. Swain S, Clise-Dwyer K, Haynes L. Homeostasis and the age-associated defect of CD4 T cells. Semin Immunol. 2005;17:370-7.
43. Song H, Price PW, Cerny J. Age-related changes in antibody repertoire: contribution from T cells. Immunol Rev. 1997;160:55-62.
44. Zheng B, Han S, Takahashi Y, Kelsoe G. Immunosenescence and germinal center reaction. Immunol Rev. 1997;160:63-77.
45. Frasca D, Landin AM, Riley RL, Blomberg BB. Mechanisms for decreased function of B cells in aged mice and humans. J Immunol. 2008;180:2741-6.
46. Frasca D, Riley RL, Blomberg BB. Aging murine B cells have decreased class switch induced by anti-CD40 or BAFF. Exp Gerontol. 2007;42:192-203.
47. Frasca D, Van der Put E, Riley RL, Blomberg BB. Reduced Ig class switch in aged mice correlates with decreased E47 and activation-induced cytidine deaminase. J Immunol. 2004;172:2155-62.
48. Yang X, Stedra J, Cerny J. Relative contribution of T and B cells to hypermutation and selection of the antibody repertoire in germinal centers of aged mice. J Exp Med. 1996;183(3):959-70.
49. Frasca D, Landin AM, Lechner SC, Ryan JG, Schwartz R, Riley RL, Blomberg BB. Aging down-regulates the transcription factor E2A, activation-induced cytidine deaminase, and Ig class switch in human B cells. J Immunol. 2008;180:5283-90.
50. Chahwan R, Edelmann W, Scharff MD, Roa S. AIDing antibody diversity by error-prone mismatch repair. Semin Immunol. 2012;24:293-300.
51. Frasca D, Romero M, Diaz A, Alter-Wolf S, Ratliff M, Landin A, Riley R, Blomberg B. A molecular mechanism for TNF-alpha-mediated downregulation of B cell responses. J Immunol. 2012;188:279-86.
52. Klinman NR, Kline GH the B-cell biology of aging. Immunol Rev. 1997;160:103-14.
53. Nicoletti C, Borghesi-Nicoletti C, Yang XH, Schulze DH, Cerny J. Repertoire diversity of antibody response to bacterial antigens in aged mice. II. Phosphorylcholine-antibody in young and aged mice differ in both VH/VL gene repertoire and in specificity. J Immunol. 1991;147:2750-5.
54. Riley SC, Froscher BG, Linton PJ, Zharhary D, Marcu K, Klinman NR. Altered VH gene segment utilization in the response to phosphorylcholine by aged mice. J Immunol. 1989;143:3798-805.
55. Zharhary D, Klinman NR. B cell repertoire diversity to PR8 influenza virus does not decrease with age. J Immunol. 1984;133:2285-7.
56. Zharhary D, Klinman NR the frequency and fine specificity of B cells responsive to (4-hydroxy-3-nitrophenyl)acetyl in aged mice. Cell Immunol. 1986;100:452-61.
57. Gibson KL, Wu YC, Barnett Y, Duggan O, Vaughan R, Kondeatis E, Nilsson BO, Wikby A, Kipling D, Dunn-Walters DK. B-cell diversity decreases in old age and is correlated with poor health status. Aging Cell. 2009;8:18-25.
58. H gene repertoire of developing precursor B lymphocytes in mouse bone marrow mediated by the pre-B cell receptor. Immunity. 1997;7:357-68.
59. Kline GH, Hartwell L, Beck-Engeser GB, Keyna U, Zaharevitz S, Klinman NR, Jäck HM. Pre-B cell receptor-mediated selection of pre-B cells synthesizing functional mu heavy chains. J Immunol. 1998;161:1608-18.
60. Keyna U, Beck-Engeser GB, Jongstra J, Applequist SE, Jack HM. Surrogate light chain-dependent selection of Ig heavy chain V regions. J Immunol. 1995;155:55365542.
61. Ye J, McCray SK, Clarke SH the transition of pre-B1 to pre-BII cells is dependent on the VH structure of the μ/surrogate L chain receptor. EMBO J. 1996;15:1524-33.
62. Keenan RA, De Riva A, Corleis B, Hepburn L, Licence S, Winkler TH, Mårtensson IL. Censoring of autoreactive B cell development by the pre-B cell receptor. Science. 2008;321:696-9.
63. Alter-Wolf S, Blomberg BB, Riley RL. Deviation of the B cell pathway in senescent mice is associated with reduced surrogate light chain expression and altered immature B cell generation, phenotype, and light chain expression. J Immunol. 2009;182:138-47.
64. Wols HA, Johnson KM, Ippolito JA, Birjandi SZ, Su Y, Le PT, Witte PL. Migration of immature and mature B cells in the aged microenvironment. Immunology. 2010;129:278-90.
65. Kline GH, Hayden TA, Klinman NR. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J Immunol. 1999;162:3342-9.
66. Johnson SA, Rozzo SJ, Cambier JC. Aging-dependent exclusion of antigen-inexperienced cells from the peripheral B cell repertoire. J Immunol. 2002;168:5014-23.
67. Keren Z, Naor S, Nussbaum S, Golan K, Itkin T, Sasaki Y, Schmidt-Supprian M, Lapidot T, Melamed D. B-cell depletion reactivates B lymphopoiesis in the BM and rejuvenates the B lineage in aging. Blood. 2011;117:3104-12.
68. Keren Z, Averbuch D, Shahaf G, Zisman-Rozen S, Golan K, Itkin T, Lapidot T, Mehr R, Melamed D. Chronic B cell deficiency from birth prevents age-related alterations in the B lineage. J Immunol. 2011;187:2140-7.
69. Van Den Broeck A, Cambier J. B cells talk to their progenitors. Blood. 2011;117:2985-6.
70. Yanaba K. Bouaziz J.-D., Matsushita T, Tsubata T, Tedder TF the development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol. 2009;182:7459-72.
71. + bone marrow fraction are increased in senescence and reduce E2A and surrogate light chain proteins in B cell precursors. Mech Ageing Dev. 2009;130:384-92.