CoChat
Sign Up
Cited by 131Hematopoietic Stem Cell TransplantationMultiple Myeloma Research and TreatmentsImmune cells in cancer

Plasma cells are obligate effectors of enhanced myelopoiesis in aging bone marrow

Open access
Pioli, Peter D., Casero, David, Montecino-Rodriguez, Encarnacion, Morrison, Sherie L., Dorshkind, Kenneth·2019·Immunity
DOI 10.1016/j.immuni.2019.06.006PMC PMC6703913
Open this paper in CoChat — free accountOpen PDF

Abstract

Aging results in increased myelopoiesis, which is linked to the increased incidence of myeloid leukemias and production of myeloid-derived suppressor cells. Here, we examined the contribution of plasma cells (PCs) to age-related increases in myelopoiesis, as PCs exhibit immune regulatory function and sequester in bone marrow (BM). PC number was increased in old BM, and they exhibited high expression of genes encoding inflammatory cytokines and pathogen sensors. Antibody-mediated depletion of PCs from old mice reduced the number of myeloid-biased hematopoietic stem cells and mature myeloid cells to levels in young animals, but lymphopoiesis was not rejuvenated, indicating that redundant mechanisms inhibit that process. PCs also regulated the production of inflammatory factors from BM stromal cells, and disruption of the PC-stromal cell circuitry with inhibitors of the cytokines IL-1 and TNF-α attenuated myelopoiesis in old mice. Thus, the age-related increase in myelopoiesis is driven by an inflammatory network orchestrated by PCs.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.immuni.2019.06.006

Cites

16 of 16 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Increased IL-1 BM level is a hallmark of hematopoietic inflammaging in mice.

    “Increased IL-1 BM level, produced by different cellular sources, is a hallmark of hematopoietic inflammaging in mice.21,22,42”

    From Aging drives <i>Tet2</i> <i>+/−</i> clonal hematopoiesis via IL-1 signaling (2023) · cites this paper as [22]

    The Discussion reports an age-dependent increase in Il1b expression in bone-marrow stroma and identifies plasma cells as another potential IL-1 source in old mice. This supports the link between IL-1 and hematopoietic inflammaging, but the cited passages do not establish an increased IL-1 protein level in bone marrow. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 113

  1. Alter-Wolf S, Blomberg BB, and Riley RL (2009). Old mice retain bone marrow B1 progenitors, but lose B2 precursors, and exhibit altered immature B cell phenotype and light chain usage. Mechanisms of ageing and development 130, 401– 408. 19428460 PMC2734388
  2. Baldridge MT, King KY, and Goodell MA (2011). Inflammatory signals regulate hematopoietic stem cells. Trends in immunology 32, 57– 65. 21233016 PMC3042730
  3. Baratono SR, Chu N, Richman LP, and Behrens EM (2015). Toll-like receptor 9 and interferon-gamma receptor signaling suppress the B-cell fate of uncommitted progenitors in mice. European journal of immunology 45, 1313– 1325. 25639361 PMC4913483
  4. Beerman I, Bhattacharya D, Zandi S, Sigvardsson M, Weissman IL, Bryder D, and Rossi DJ (2010). Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proceedings of the National Academy of Sciences of the United States of America 107, 5465– 5470. 20304793 PMC2851806
  5. Benz C, Copley MR, Kent DG, Wohrer S, Cortes A, Aghaeepour N, Ma E, Mader H, Rowe K, Day C, (2012). Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell stem cell 10, 273– 283. 22385655
  6. Bermejo DA, Jackson SW, Gorosito-Serran M, Acosta-Rodriguez EV, Amezcua-Vesely MC, Sather BD, Singh AK, Khim S, Mucci J, Liggitt D, (2013). Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORgammat and Ahr that leads to IL-17 production by activated B cells. Nature immunology 14, 514– 522. 23563688 PMC3631452
  7. Boulais PE, and Frenette PS (2015). Making sense of hematopoietic stem cell niches. Blood 125, 2621– 2629. 25762174 PMC4408288
  8. Casero D, Sandoval S, Seet CS, Scholes J, Zhu Y, Ha VL, Luong A, Parekh C, and Crooks GM (2015). Long non-coding RNA profiling of human lymphoid progenitor cells reveals transcriptional divergence of B cell and T cell lineages. Nature immunology 16, 1282– 1291. 26502406 PMC4653072
  9. Challen GA, Boles NC, Chambers SM, and Goodell MA (2010). Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell stem cell 6, 265– 278. 20207229 PMC2837284
  10. Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, and Goodell MA (2007). Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS biology 5, e201. 17676974 PMC1925137
  11. Chang J, Wang Y, Shao L, Laberge RM, Demaria M, Campisi J, Janakiraman K, Sharpless NE, Ding S, Feng W, (2016). Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice. Nature medicine 22, 78– 83. PMC4762215 26657143
  12. Chen X, Deng H, Churchill MJ, Luchsinger LL, Du X, Chu TH, Friedman RA, Middelhoff M, Ding H, Tailor YH, (2017). Bone Marrow Myeloid Cells Regulate Myeloid-Biased Hematopoietic Stem Cells via a Histamine-Dependent Feedback Loop. Cell stem cell 21, 747– 760 e747. 29198940 PMC5975960
  13. Chernova I, Jones DD, Wilmore JR, Bortnick A, Yucel M, Hershberg U, and Allman D (2014). Lasting antibody responses are mediated by a combination of newly formed and established bone marrow plasma cells drawn from clonally distinct precursors. Journal of immunology 193, 4971– 4979. PMC4234148 25326027
  14. Choi JS, and Harley BA (2017). Marrow-inspired matrix cues rapidly affect early fate decisions of hematopoietic stem and progenitor cells. Science advances 3, e1600455. 28070554 PMC5218514
  15. Chu VT, and Berek C (2013). The establishment of the plasma cell survival niche in the bone marrow. Immunological reviews 251, 177– 188. 23278749
  16. Cocco C, Morandi F, and Airoldi I (2011). Interleukin-27 and interleukin-23 modulate human plasmacell functions. Journal of leukocyte biology 89, 729– 734. 21330353
  17. Conley ME, and Cooper MD (1981). Immature IgA B cells in IgA-deficient patients. The New England journal of medicine 305, 495– 497. 6973088
  18. Cordeiro Gomes A, Hara T, Lim VY, Herndler-Brandstetter D, Nevius E, Sugiyama T, Tani-Ichi S, Schlenner S, Richie E, Rodewald HR, (2016). Hematopoietic Stem Cell Niches Produce Lineage-Instructive Signals to Control Multipotent Progenitor Differentiation. Immunity 45, 1219– 1231. 27913094 PMC5538583
  19. Dang VD, Hilgenberg E, Ries S, Shen P, and Fillatreau S (2014). From the regulatory functions of B cells to the identification of cytokine-producing plasma cell subsets. Current opinion in immunology 28, 77– 83. 24637161
  20. Das A, Arifuzzaman S, Yoon T, Kim SH, Chai JC, Lee YS, Jung KH, and Chai YG (2017). RNA sequencing reveals resistance of TLR4 ligand-activated microglial cells to inflammation mediated by the selective jumonji H3K27 demethylase inhibitor. Scientific reports 7, 6554. 28747667 PMC5529413
  21. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, and Gingeras TR (2013). STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15– 21. 23104886 PMC3530905
  22. Dorshkind K (1988a). IL-1 inhibits B cell differentiation in long term bone marrow cultures. Journal of immunology 141, 531– 538. 3260256
  23. Dorshkind K (1988b). Interleukin-1 inhibition of B lymphopoiesis is reversible. Blood 72, 2053– 2055. 3264197
  24. Dorshkind K (1991). In vivo administration of recombinant granulocyte-macrophage colony-stimulating factor results in a reversible inhibition of primary B lymphopoiesis. Journal of immunology 146, 4204– 4208. 2040797
  25. Dykstra B, and de Haan G (2008). Hematopoietic stem cell aging and self-renewal. Cell and tissue research 331, 91– 101. 18008087
  26. Ergen AV, Boles NC, and Goodell MA (2012). Rantes/Ccl5 influences hematopoietic stem cell subtypes and causes myeloid skewing. Blood 119, 2500– 2509. 22289892 PMC3311273
  27. Fairfax KA, Kallies A, Nutt SL, and Tarlinton DM (2008). Plasma cell development: from B-cell subsets to long-term survival niches. Seminars in immunology 20, 49– 58. 18222702
  28. Fang MM, Barman PK, Thiruppathi M, Mirza RE, McKinney RD, Deng J, Christman JW, Du X, Fukai T, Ennis WJ, (2018). Oxidant Signaling Mediated by Nox2 in Neutrophils Promotes Regenerative Myelopoiesis and Tissue Recovery following Ischemic Damage. Journal of immunology 201, 2414– 2426. PMC6258003 30201810
  29. Flores RR, Clauson CL, Cho J, Lee BC, McGowan SJ, Baker DJ, Niedernhofer LJ, and Robbins PD (2017). Expansion of myeloid-derived suppressor cells with aging in the bone marrow of mice through a NF-kappaB-dependent mechanism. Aging cell 16, 480– 487. 28229533 PMC5418207
  30. Fowler T, Garruss AS, Ghosh A, De S, Becker KG, Wood WH, Weirauch MT, Smale ST, Aronow B, Sen R, and Roy AL (2015). Divergence of transcriptional landscape occurs early in B cell activation. Epigenetics & chromatin 8, 20. 25987903 PMC4434543
  31. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, and De Benedictis G (2000). Inflamm-aging. An evolutionary perspective on immunosenescence. Annals of the New York Academy of Sciences 908, 244– 254. 10911963
  32. Fritz JH, Rojas OL, Simard N, McCarthy DD, Hapfelmeier S, Rubino S, Robertson SJ, Larijani M, Gosselin J, Ivanov II, (2011). Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut. Nature 481, 199– 203. 22158124 PMC3487691
  33. Geiger H, de Haan G, and Florian MC (2013). The ageing haematopoietic stem cell compartment. Nature reviews. Immunology 13, 376– 389. 23584423
  34. Geiger H, and Van Zant G (2002). The aging of lympho-hematopoietic stem cells. Nature immunology 3, 329– 333. 11919569
  35. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, and Sansonetti PJ (2003). Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. The Journal of biological chemistry 278, 8869– 8872. 12527755
  36. Guidi N, and Geiger H (2017). Rejuvenation of aged hematopoietic stem cells. Seminars in hematology 54, 51– 55. 28088989 PMC5244470
  37. Guidi N, Sacma M, Standker L, Soller K, Marka G, Eiwen K, Weiss JM, Kirchhoff F, Weil T, Cancelas JA, (2017). Osteopontin attenuates aging-associated phenotypes of hematopoietic stem cells. The EMBO journal 36, 840– 853. 28254837 PMC5376966
  38. Hardy RR, Carmack CE, Shinton SA, Kemp JD, and Hayakawa K (1991). Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. The Journal of experimental medicine 173, 1213– 1225. 1827140 PMC2118850
  39. Hardy RR, and Hayakawa K (1995). B-lineage differentiation stages resolved by multiparameter flow cytometry. Annals of the New York Academy of Sciences 764, 19– 24. 7486522
  40. Henry CJ, Casas-Selves M, Kim J, Zaberezhnyy V, Aghili L, Daniel AE, Jimenez L, Azam T, McNamee EN, Clambey ET, (2015). Aging-associated inflammation promotes selection for adaptive oncogenic events in B cell progenitors. The Journal of clinical investigation 125, 4666– 4680. 26551682 PMC4665776
  41. Hirata Y, Furuhashi K, Ishii H, Li HW, Pinho S, Ding L, Robson SC, Frenette PS, and Fujisaki J (2018). CD150(high) Bone Marrow Tregs Maintain Hematopoietic Stem Cell Quiescence and Immune Privilege via Adenosine. Cell stem cell 22, 445– 453 e445. 29456159 PMC6534147
  42. Hoggatt J, Kfoury Y, and Scadden DT (2016). Hematopoietic Stem Cell Niche in Health and Disease. Annual review of pathology 11, 555– 581. 27193455
  43. Hu X, Garcia M, Weng L, Jung X, Murakami JL, Kumar B, Warden CD, Todorov I, and Chen CC (2016). Identification of a common mesenchymal stromal progenitor for the adult haematopoietic niche. Nature communications 7, 13095. PMC5062560 27721421
  44. Jalkanen M, Nguyen H, Rapraeger A, Kurn N, and Bernfield M (1985). Heparan sulfate proteoglycans from mouse mammary epithelial cells: localization on the cell surface with a monoclonal antibody. The Journal of cell biology 101, 976– 984. 3161899 PMC2113719
  45. Kawai T, and Akira S (2010). The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature immunology 11, 373– 384. 20404851
  46. Kayaba A, Itoh-Nakadai A, Niibe K, Shirota M, Funayama R, Sugahara-Tobinai A, Wong YL, Inui M, Nakayama K, and Takai T (2018). Bone Marrow PDGFR+Sca-1+ Enriched Mesenchymal Stem Cells Support Survival of and Antibody Production by Plasma Cells in vitro through IL-6. International immunology. 29529192
  47. Kennedy DE, and Knight KL (2015). Inhibition of B Lymphopoiesis by Adipocytes and IL-1-Producing Myeloid-Derived Suppressor Cells. Journal of immunology 195, 2666– 2674. PMC4561202 26268654
  48. Kennedy DE, and Knight KL (2017). Inflammatory Changes in Bone Marrow Microenvironment Associated with Declining B Lymphopoiesis. Journal of immunology 198, 3471– 3479. PMC5435233 28320833
  49. Kim HM, Jeong CS, Choi HS, Kawada T, and Yu R (2011). LIGHT/TNFSF14 enhances adipose tissue inflammatory responses through its interaction with HVEM. FEBS letters 585, 579– 584. 21236258
  50. Kim MS, and Kim TS (2014). IgA+ plasma cells in murine intestinal lamina propria as a positive regulator of Treg differentiation. Journal of leukocyte biology 95, 461– 469. 24231258
  51. King AM, Keating P, Prabhu A, Blomberg BB, and Riley RL (2009). NK cells in the CD19− B220+ bone marrow fraction are increased in senescence and reduce E2A and surrogate light chain proteins in B cell precursors. Mechanisms of ageing and development 130, 384– 392. 19428458 PMC2743292
  52. King KY, and Goodell MA (2011). Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nature reviews. Immunology 11, 685– 692. PMC4154310 21904387
  53. Kofoed EM, and Vance RE (2011). Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477, 592– 595. 21874021 PMC3184209
  54. Kovtonyuk LV, Fritsch K, Feng X, Manz MG, and Takizawa H (2016). Inflamm-Aging of Hematopoiesis, Hematopoietic Stem Cells, and the Bone Marrow Microenvironment. Frontiers in immunology 7, 502. 27895645 PMC5107568
  55. Kunisawa J, Gohda M, Hashimoto E, Ishikawa I, Higuchi M, Suzuki Y, Goto Y, Panea C, Ivanov II, Sumiya R, (2013). Microbe-dependent CD11b+ IgA+ plasma cells mediate robust early-phase intestinal IgA responses in mice. Nature communications 4, 1772. PMC3644083 23612313
  56. Lam WY, Jash A, Yao CH, D’Souza L, Wong R, Nunley RM, Meares GP, Patti GJ, and Bhattacharya D (2018). Metabolic and Transcriptional Modules Independently Diversify Plasma Cell Lifespan and Function. Cell reports 24, 2479– 2492 e2476. 30157439 PMC6172041
  57. Lemke A, Kraft M, Roth K, Riedel R, Lammerding D, and Hauser AE (2016). Long-lived plasma cells are generated in mucosal immune responses and contribute to the bone marrow plasma cell pool in mice. Mucosal immunology 9, 83– 97. 25943272
  58. Lo Celso C, and Scadden DT (2011). The haematopoietic stem cell niche at a glance. Journal of cell science 124, 3529– 3535. 22083139 PMC3215569
  59. Lopez D, Montoya D, Ambrose M, Lam L, Briscoe L, Adams C, Modlin RL, and Pellegrini M (2017). SaVanT: a web-based tool for the sample-level visualization of molecular signatures in gene expression profiles. BMC genomics 18, 824. 29070035 PMC5657101
  60. Love MI, Huber W, and Anders S (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology 15, 550. 25516281 PMC4302049
  61. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, and Flavell RA (2004). Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proceedings of the National Academy of Sciences of the United States of America 101, 5598– 5603. 15034168 PMC397437
  62. Luo Y, Shao L, Chang J, Feng W, Liu YL, Cottler-Fox MH, Emanuel PD, Hauer-Jensen M, Bernstein ID, Liu L, (2018). M1 and M2 macrophages differentially regulate hematopoietic stem cell self-renewal and ex vivo expansion. Blood advances 2, 859– 870. 29666049 PMC5916005
  63. Maeda K, Baba Y, Nagai Y, Miyazaki K, Malykhin A, Nakamura K, Kincade PW, Sakaguchi N, and Coggeshall KM (2005). IL-6 blocks a discrete early step in lymphopoiesis. Blood 106, 879– 885. 15831701 PMC1761686
  64. Miller JP, and Allman D (2003). The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. Journal of immunology 171, 2326– 2330. 12928378
  65. Minges Wols HA, Underhill GH, Kansas GS, and Witte PL (2002). The role of bone marrow-derived stromal cells in the maintenance of plasma cell longevity. Journal of immunology 169, 4213– 4221. 12370351
  66. Mirantes C, Passegue E, and Pietras EM (2014). Pro-inflammatory cytokines: emerging players regulating HSC function in normal and diseased hematopoiesis. Experimental cell research 329, 248– 254. 25149680 PMC4250307
  67. Mokhtari Z, Mech F, Zehentmeier S, Hauser AE, and Figge MT (2015). Quantitative image analysis of cell colocalization in murine bone marrow. Cytometry. Part A: the journal of the International Society for Analytical Cytology 87, 503– 512. 25652548
  68. Montecino-Rodriguez E, Kong Y, Casero D, Rouault A, Dorshkind K, and Pioli PD (2019). Lymphoid-Biased Hematopoietic Stem Cells Are Maintained with Age and Efficiently Generate Lymphoid Progeny. Stem cell reports. PMC6409485 30799276
  69. Mossadegh-Keller N, Sarrazin S, Kandalla PK, Espinosa L, Stanley ER, Nutt SL, Moore J, and Sieweke MH (2013). M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 497, 239– 243. 23575636 PMC3679883
  70. Muller-Sieburg CE, Cho RH, Karlsson L, Huang JF, and Sieburg HB (2004). Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood 103, 4111– 4118. 14976059
  71. Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, Takatsu K, and Kincade PW (2006). Toll like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24, 801– 812. 16782035 PMC1626529
  72. Nakamura-Ishizu A, Takubo K, Fujioka M, and Suda T (2014). Megakaryocytes are essential for HSC quiescence through the production of thrombopoietin. Biochemical and biophysical research communications 454, 353– 357. 25451253
  73. Nakao Y, Funami K, Kikkawa S, Taniguchi M, Nishiguchi M, Fukumori Y, Seya T, and Matsumoto M (2005). Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. Journal of immunology 174, 1566– 1573. 15661917
  74. O’Reilly SM, and Moynagh PN (2003). Regulation of Toll-like receptor 4 signalling by A20 zinc finger protein. Biochemical and biophysical research communications 303, 586– 593. 12659860
  75. Oduro KA Jr., Liu F, Tan Q, Kim CK, Lubman O, Fremont D, Mills JC, and Choi K (2012). Myeloid skewing in murine autoimmune arthritis occurs in hematopoietic stem and primitive progenitor cells. Blood 120, 2203– 2213. 22855602 PMC3447779
  76. Panopoulos AD, Bartos D, Zhang L, and Watowich SS (2002). Control of myeloid-specific integrin alpha Mbeta 2 (CD11b/CD18) expression by cytokines is regulated by Stat3-dependent activation of PU.1. The Journal of biological chemistry 277, 19001– 19007. 11889125 PMC2388249
  77. Panopoulos AD, Zhang L, Snow JW, Jones DM, Smith AM, El Kasmi KC, Liu F, Goldsmith MA, Link DC, Murray PJ, and Watowich SS (2006). STAT3 governs distinct pathways in emergency granulopoiesis and mature neutrophils. Blood 108, 3682– 3690. 16888100 PMC1895456
  78. Pietras EM, Mirantes-Barbeito C, Fong S, Loeffler D, Kovtonyuk LV, Zhang S, Lakshminarasimhan R, Chin CP, Techner JM, Will B, (2016). Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nature cell biology 18, 607– 618. 27111842 PMC4884136
  79. Pinto D, Montani E, Bolli M, Garavaglia G, Sallusto F, Lanzavecchia A, and Jarrossay D (2013). A functional BCR in human IgA and IgM plasma cells. Blood 121, 4110– 4114. 23550036
  80. Poulos MG, Ramalingam P, Gutkin MC, Llanos P, Gilleran K, Rabbany SY, and Butler JM (2017). Endothelial transplantation rejuvenates aged hematopoietic stem cell function. The Journal of clinical investigation 127, 4163– 4178. 29035282 PMC5663355
  81. Puchta A, Naidoo A, Verschoor CP, Loukov D, Thevaranjan N, Mandur TS, Nguyen PS, Jordana M, Loeb M, Xing Z, (2016). TNF Drives Monocyte Dysfunction with Age and Results in Impaired Anti-pneumococcal Immunity. PLoS pathogens 12, e1005368. 26766566 PMC4713203
  82. Qi Y, Goel R, Kim S, Richards EM, Carter CS, Pepine CJ, Raizada MK, and Buford TW (2017). Intestinal Permeability Biomarker Zonulin is Elevated in Healthy Aging. Journal of the American Medical Directors Association 18, 810 e811– 810 e814. PMC5581307 28676292
  83. Qureshi ST, Gros P, and Malo D (1999). The Lps locus: genetic regulation of host responses to bacterial lipopolysaccharide. Inflammation research: official journal of the European Histamine Research Society... [ ] 48, 613– 620. 10669111
  84. Ratliff M, Alter S, Frasca D, Blomberg BB, and Riley RL (2013). In senescence, age-associated B cells secrete TNFalpha and inhibit survival of B-cell precursors. Aging cell 12, 303– 311. 23410004 PMC3716274
  85. Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, Tiglao E, Figueiredo JL, Iwamoto Y, Theurl I, (2012). Innate response activator B cells protect against microbial sepsis. Science 335, 597– 601. 22245738 PMC3279743
  86. Reynolds AE, Kuraoka M, and Kelsoe G (2015). Natural IgM is produced by CD5-plasma cells that occupy a distinct survival niche in bone marrow. Journal of immunology 194, 231– 242. PMC4272881 25429072
  87. Rossi DJ, Bryder D, and Weissman IL (2007). Hematopoietic stem cell aging: mechanism and consequence. Experimental gerontology 42, 385– 390. 17275237 PMC1892213
  88. Rundberg Nilsson A, Soneji S, Adolfsson S, Bryder D, and Pronk CJ (2016). Human and Murine Hematopoietic Stem Cell Aging Is Associated with Functional Impairments and Intrinsic Megakaryocytic/Erythroid Bias. PloS one 11, e0158369. 27368054 PMC4930192
  89. Schepers K, Hsiao EC, Garg T, Scott MJ, and Passegue E (2012). Activated Gs signaling in osteoblastic cells alters the hematopoietic stem cell niche in mice. Blood 120, 3425– 3435. 22859604 PMC3482855
  90. Schmitt TM, and Zuniga-Pflucker JC (2002). Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17, 749– 756. 12479821
  91. Shaikh RB, Santee S, Granger SW, Butrovich K, Cheung T, Kronenberg M, Cheroutre H, and Ware CF (2001). Constitutive expression of LIGHT on T cells leads to lymphocyte activation, inflammation, and tissue destruction. Journal of immunology 167, 6330– 6337. 11714797
  92. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, and Ideker T (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research 13, 2498– 2504. 14597658 PMC403769
  93. Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, and Calame K (2003). Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19, 607– 620. 14563324
  94. Shen P, Roch T, Lampropoulou V, O’Connor RA, Stervbo U, Hilgenberg E, Ries S, Dang VD, Jaimes Y, Daridon C, (2014). IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 507, 366– 370. 24572363 PMC4260166
  95. Shi W, Liao Y, Willis SN, Taubenheim N, Inouye M, Tarlinton DM, Smyth GK, Hodgkin PD, Nutt SL, and Corcoran LM (2015). Transcriptional profiling of mouse B cell terminal differentiation defines a signature for antibody-secreting plasma cells. Nature immunology 16, 663– 673. 25894659
  96. Skokowa J, Lan D, Thakur BK, Wang F, Gupta K, Cario G, Brechlin AM, Schambach A, Hinrichsen L, Meyer G, (2009). NAMPT is essential for the G-CSF-induced myeloid differentiation via a NAD(+)-sirtuin-1-dependent pathway. Nature medicine 15, 151– 158. 19182797
  97. Sugiyama T, Kohara H, Noda M, and Nagasawa T (2006). Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25, 977– 988. 17174120
  98. Suzuki-Yamazaki N, Yanobu-Takanashi R, Okamura T, and Takaki S (2017). IL-10 production in murine IgM(+) CD138(hi) cells is driven by Blimp-1 and downregulated in class-switched cells. European journal of immunology 47, 493– 503. 28012163
  99. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, and Akira S (1999). Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11, 443– 451. 10549626
  100. Tang D, Tao S, Chen Z, Koliesnik IO, Calmes PG, Hoerr V, Han B, Gebert N, Zornig M, Loffler B, (2016). Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging. The Journal of experimental medicine 213, 535– 553. 26951333 PMC4821645
  101. Taubenheim N, Tarlinton DM, Crawford S, Corcoran LM, Hodgkin PD, and Nutt SL (2012). High rate of antibody secretion is not integral to plasma cell differentiation as revealed by XBP-1 deficiency. Journal of immunology 189, 3328– 3338. 22925926
  102. Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP, Loukov D, Schenck LP, Jury J, Foley KP, (2017). Age-Associated Microbial Dysbiosis Promotes Intestinal Permeability, Systemic Inflammation, and Macrophage Dysfunction. Cell host & microbe 21, 455– 466 e454. 28407483 PMC5392495
  103. Tripathi S, Pohl MO, Zhou Y, Rodriguez-Frandsen A, Wang G, Stein DA, Moulton HM, DeJesus P, Che J, Mulder LC, (2015). Meta- and Orthogonal Integration of Influenza “OMICs” Data Defines a Role for UBR4 in Virus Budding. Cell host & microbe 18, 723– 735. 26651948 PMC4829074
  104. Tsujimoto T, Lisukov IA, Huang N, Mahmoud MS, and Kawano MM (1996). Plasma cells induce apoptosis of pre-B cells by interacting with bone marrow stromal cells. Blood 87, 3375– 3383. 8605355
  105. Tung JW, Mrazek MD, Yang Y, Herzenberg LA, and Herzenberg LA (2006). Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proceedings of the National Academy of Sciences of the United States of America 103, 6293– 6298. 16606838 PMC1458871
  106. Ueda Y, Kondo M, and Kelsoe G (2005). Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. The Journal of experimental medicine 201, 1771– 1780. 15939792 PMC1952536
  107. Walkley CR, Olsen GH, Dworkin S, Fabb SA, Swann J, McArthur GA, Westmoreland SV, Chambon P, Scadden DT, and Purton LE (2007a). A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 129, 1097– 1110. 17574023 PMC1974882
  108. Walkley CR, Shea JM, Sims NA, Purton LE, and Orkin SH (2007b). Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129, 1081– 1095. 17574022 PMC2768301
  109. Yazdani R, Azizi G, Abolhassani H, and Aghamohammadi A (2017). Selective IgA Deficiency: Epidemiology, Pathogenesis, Clinical Phenotype, Diagnosis, Prognosis and Management. Scandinavian journal of immunology 85, 3– 12. 27763681
  110. Zehentmeier S, Roth K, Cseresnyes Z, Sercan O, Horn K, Niesner RA, Chang HD, Radbruch A, and Hauser AE (2014). Static and dynamic components synergize to form a stable survival niche for bone marrow plasma cells. European journal of immunology 44, 2306– 2317. 24777940
  111. Zhang J, Dai J, Lu Y, Yao Z, O’Brien CA, Murtha JM, Qi W, Hall DE, Manolagas SC, Ershler WB, and Keller ET (2004). In vivo visualization of aging-associated gene transcription: evidence for free radical theory of aging. Experimental gerontology 39, 239– 247. 15036418
  112. Zhou A, Li M, He B, Feng W, Huang F, Xu B, Dunker AK, Balch C, Li B, Liu Y, and Wang Y (2016). Lipopolysaccharide treatment induces genome-wide pre-mRNA splicing pattern changes in mouse bone marrow stromal stem cells. BMC genomics 17 Suppl 7, 509. 27557078 PMC5001229
  113. Ziegler P, Boettcher S, Takizawa H, Manz MG, and Brummendorf TH (2016). LPS-stimulated human bone marrow stroma cells support myeloid cell development and progenitor cell maintenance. Annals of hematology 95, 173– 178. 26555286

Cited by

Sorted by citations

Authors
Pioli, P. D., Casero, D., Montecino-Rodriguez, E., Morrison, S. L., & Dorshkind, K.
Affiliations
University of California, Los Angeles (US)
Corresponding author
Dorshkind, Kenneth
ORCID
Venue
Immunity
Publisher
Elsevier BV
Published
2019-08
Volume
51
Issue
2
Pages
351-366.e6
ISSN
1074-7613 (ISSN-L)
DOI
10.1016/j.immuni.2019.06.006
PMC
PMC6703913
OpenAlex
W2958299423
Cited by
131
References
16
Citations by year
2026: 10 · 2025: 25 · 2024: 26 · 2023: 17 · 2022: 17 · 2021: 18 · 2020: 13 · 2019: 5
FWCI
9.37
Type
journal article
Language
en
Open access
Licence
Locations
  • Immunity (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
National Institutes of Health
Topics
  • Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
  • Health Sciences › Medicine › Hematology › Multiple Myeloma Research and Treatments
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords
plasma cells, myelopoiesis, bone marrow aging, hematopoietic stem cells, myeloid leukemia, myeloid-derived suppressor cells, mesenchymal stem cells, inflammation, interleukin-1, TNF-α, lymphocyte development, immune regulation
MeSH terms
Aging, Animals, Bone Marrow, Cells, Cultured, Hematopoietic Stem Cells, Humans, Inflammation, Interleukin-1, Lymphocyte Depletion, Mice, Inbred C57BL, Mice, Transgenic, Plasma Cells, Tumor Necrosis Factor-alpha, Myelopoiesis, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review