Quantitative and qualitative analysis of bone marrow CD8+ T cells from different bones uncovers a major contribution of the bone marrow in the vertebrae

Frontiers in Immunology

Volumn 6, Issue JAN, 2016, Pages

  Geerman, Sulima ^a,b   Hickson, Sarah ^a,b   Brasser, Giso ^a,b   Pascutti, Maria Fernanda ^a,b   Nolte, Martijn A ^a,b  

^a SANQUIN RESEARCH   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Bone marrow; CD69; CD8+ T cells; Ki 67; LCMV; Memory; Tissue resident; Vertebrae

Indexed keywords

CD69 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 15 RECEPTOR; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; KI 67 ANTIGEN; L SELECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE; BONE MARROW; CALVARIA; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CENTRAL MEMORY; CONTROLLED STUDY; EFFECTOR MEMORY; FEMUR; FLOW CYTOMETRY; HUMERUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY; MOUSE; NONHUMAN; PELVIS; PHENOTYPE; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RADIUS; SPLEEN; STERNUM; TIBIA; VERTEBRA;

EID: 84958172652     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00660     Document Type: Article

References (42)

1. Bianco P. Bone and the hematopoietic niche: a tale of two stem cells. Blood (2011) 117:5281-9. doi: 10.1182/blood-2011-01-315069
2. Gurkan UA, Akkus O. The mechanical environment of bone marrow: a review. Ann Biomed Eng (2008) 36:1978-91. doi:10.1007/s10439-008-9577-x
3. Guezguez B, Campbell CJV, Boyd AL, Karanu F, Casado FL, Di Cresce C, et al. Regional localization within the bone marrow influences the functional capacity of human HSCs. Cell Stem Cell (2013) 13:175-89. doi:10.1016/j.stem.2013.06.015
4. Farrell TL, McGuire TR, Bilek LD, Brusnahan SK, Jackson JD, Lane JT, et al. Changes in the frequencies of human hematopoietic stem and progenitor cells with age and site. Exp Hematol (2014) 42:146-54. doi:10.1016/j.exphem.2013.11.003
5. Lassailly F, Foster K, Lopez-onieva L, Currie E, Bonnet D. Multimodal imaging reveals structural and functional heterogeneity in different bone marrow compartments: functional implications on hematopoietic stem cells. Blood (2013) 122:1730-40. doi:10.1182/blood-2012-11-467498
6. Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M, et al. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med (2003) 9:1151-7. doi:10.1038/nm914
7. Duffy D, Perrin H, Abadie V, Benhabiles N, Boissonnas A, Liard C, et al. Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. Immunity (2012) 37:917-29. doi:10.1016/j.immuni.2012.07.015
8. Di Rosa F, Santoni A. Memory T-cell competition for bone marrow seeding. Immunology (2003) 108:296-304. doi:10.1046/j.1365-2567.2003.01593.x
9. Mazo IB, Honczarenko M, Leung H, Cavanagh LL, Bonasio R, Weninger W, et al. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity (2005) 22:259-70. doi:10.1016/j.immuni.2005.01.008
10. Tokoyoda K, Zehentmeier S, Hegazy AN, Albrecht I, Grün JR, Löhning M, et al. Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow. Immunity (2009) 30:721-30. doi:10.1016/j.immuni.2009.03.015
11. Lodolce JP, Boone DL, Chai S, Swain RE, Dassopoulos T, Trettin S, et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity (1998) 9:669-76. doi:10.1016/S1074-7613(00)80664-0
12. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med (2000) 191:771-80. doi:10.1084/jem.191.5.771
13. Schluns KS, Kieper WC, Jameson SC, Lefrançois L. Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo. Nat Immunol (2000) 1:426-32. doi:10.1038/80868
14. Pulle G, Vidric M, Watts TH. IL-15-dependent induction of 4-1BB promotes antigen-independent CD8 memory T cell survival. J Immunol (2006) 176:2739-48. doi:10.4049/jimmunol.176.5.2739
15. Snell LM, Lin GHY, Watts TH. IL-15-dependent upregulation of GITR on CD8 memory phenotype T cells in the bone marrow relative to spleen and lymph node suggests the bone marrow as a site of superior bioavailability of IL-15. J Immunol (2012) 188:5915-23. doi:10.4049/jimmunol.1103270
16. Sercan Alp Ö, Durlanik S, Schulz D, McGrath M, Grün JR, Bardua M, et al. Memory CD8+ T cells colocalize with IL-7+ stromal cells in bone marrow and rest in terms of proliferation and transcription. Eur J Immunol (2015) 45(4):975-87. doi:10.1002/eji.201445295
17. Herndler-Brandstetter D, Landgraf K, Jenewein B, Tzankov A, Brunauer R, Brunner S, et al. Human bone marrow hosts polyfunctional memory CD4+ and CD8+ T cells with close contact to IL-15-producing cells. J Immunol (2011) 186:6965-71. doi:10.4049/jimmunol.1100243
18. Di Rosa F, Pabst R. The bone marrow: a nest for migratory memory T cells. Trends Immunol (2005) 26:360-6. doi:10.1016/j.it.2005.04.011
19. Tokoyoda K, Radbruch A. Signals controlling rest and reactivation of T helper memory lymphocytes in bone marrow. Cell Mol Life Sci (2012) 69:1609-13. doi:10.1007/s00018-012-0969-6
20. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature (1999) 401:708-12. doi:10.1038/44385
21. Weninger W, Crowley MA, Manjunath N, von Andrian UH. Migratory properties of naive, effector, and memory CD8(+) T cells. J Exp Med (2001) 194:953-66. doi:10.1084/jem.194.7.953
22. Cui G, Hara T, Simmons S, Wagatsuma K, Abe A, Miyachi H, et al. Characterization of the IL-15 niche in primary and secondary lymphoid organs in vivo. Proc Natl Acad Sci U S A (2014) 111:1915-20. doi:10.1073/pnas.1318281111
23. Hara T, Shitara S, Imai K, Miyachi H, Kitano S, Yao H, et al. Identification of IL-7-producing cells in primary and secondary lymphoid organs using IL-7-GFP knock-in mice. J Immunol (2012) 189:1577-84. doi:10.4049/jimmunol.1200586
24. Quinci AC, Vitale S, Parretta E, Soriani A, Iannitto ML, Cippitelli M, et al. IL-15 inhibits IL-7Ra expression by memory-phenotype CD8+ T cells in the bone marrow. Eur J Immunol (2012) 42:1129-39. doi:10.1002/eji.201142019
25. Slifka MK, Matloubian M, Ahmed R. Bone marrow is a major site of long-term antibody production after acute viral infection. J Virol (1995) 69:1895-902.
26. Slifka MK, Whitmire JK, Ahmed R. Bone marrow contains virus-specific cytotoxic T lymphocytes. Blood (1997) 90:2103-8.
27. Binder BD, Fehr J, Hengartner H, Zinkernagel RM. Virus-induced transient bone marrow aplasia: major role of interferon-alpha/beta during acute infection with the noncytopathic lymphocytic choriomeningitis virus. J Exp Med (1997) 1997(185):517-30. doi:10.1084/jem.185.3.517
28. Subramanian A, Hegde S, Porayette P, Yon M, Hankey P, Paulson RF. Friend virus utilizes the BMP4-dependent stress erythropoiesis pathway to induce erythroleukemia. J Virol (2008) 82:382-93. doi:10.1128/JVI.02487-06
29. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol (2009) 10:524-30. doi:10.1038/ni.1718
30. Tang VA, Rosenthal KL. Intravaginal infection with herpes simplex virus type-2 (HSV-2) generates a functional effector memory T cell population that persists in the murine genital tract. J Reprod Immunol (2010) 87:39-44. doi:10.1016/j.jri.2010.06.155
31. Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, Akondy R, et al. Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med (2010) 207:553-64. doi:10.1084/jem.20090858
32. Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, et al. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol (2012) 188:4866-75. doi:10.4049/jimmunol.1200402
33. Hofmann M, Pircher H. E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. Proc Natl Acad Sci U S A (2011) 108:16741-6. doi:10.1073/pnas.1107200108
34. Wakim LM, Woodward-Davis A, Bevan MJ. Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci U S A (2010) 107:17872-9. doi:10.1073/pnas.1010201107
35. Shiow LR, Rosen DB, Brdicková N, Xu Y, An J, Lanier LL, et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature (2006) 440:540-4. doi:10.1038/nature04606
36. Mackay LK, Braun A, Macleod BL, Collins N, Tebartz C, Bedoui S, et al. Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J Immunol (2015) 194(5):2059-63. doi:10.4049/jimmunol.1402256
37. Schenkel JM, Masopust D. Tissue-resident memory T cells. Immunity (2014) 41:886-97. doi:10.1016/j.immuni.2014.12.007
38. Pritz T, Landgraf-Rauf K, Herndler-Brandstetter D, Rauf R, Lair J, Gassner R, et al. Bone marrow T cells from the femur are similar to iliac crest derived cells in old age and represent a useful tool for studying the aged immune system. Immun Ageing (2013) 10:17. doi:10.1186/1742-4933-10-17
39. Cox MA, Kahan SM, Zajac AJ. Anti-viral CD8 T cells and the cytokines that they love. Virology (2013) 435:157-69. doi:10.1016/j.virol.2012.09.012
40. Mattei F, Schiavoni G, Belardelli F, Tough DF. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J Immunol (2001) 167:1179-87. doi:10.4049/jimmunol.167.3.1179
41. Libregts SFWM, Nolte MA. Parallels between immune driven-hematopoiesis and T cell activation: 3 signals that relay inflammatory stress to the bone marrow. Exp Cell Res (2014) 329(2):239-47. doi:10.1016/j.yexcr.2014.09.016
42. Steinert EM, Schenkel JM, Fraser KA, Beura LK, Manlove LS, Igyártó BZ, et al. Quantifying memory CD8 T cells reveals regionalization of immunosurveillance. Cell (2015) 161:737-49. doi:10.1016/j.cell.2015.03.031