Lamina Propria c-kit+ Immune Precursors Reside in Human Adult Intestine and Differentiate Into Natural Killer Cells

Gastroenterology

Volumn 133, Issue 2, 2007, Pages 559-573

  Chinen, Hiroshi ^a,b   Matsuoka, Katsuyoshi ^a   Sato, Toshiro ^a   Kamada, Nobuhiko ^a   Okamoto, Susumu ^a   Hisamatsu, Tadakazu ^a   Kobayashi, Taku ^a   Hasegawa, Hirotoshi ^c   Sugita, Akira ^d   Kinjo, Fukunori ^b   Fujita, Jiro ^b   Hibi, Toshifumi ^a  

^a Division of Hematology   (Japan)

^b Rhukyu University School of Medicine   (Japan)

^c KEIO UNIVERSITY   (Japan)

^d YOKOHAMA MUNICIPAL CITIZEN'S HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD33 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CD56 ANTIGEN; CYTOKINE; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR ALPHA; LYMPHOTOXIN; STEM CELL FACTOR RECEPTOR;

ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LAMINA PROPRIA; LYMPHOCYTE; MONONUCLEAR CELL; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 34547538202     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2007.05.017     Document Type: Article

References (59)

1. Akashi K., Traver D., Miyamoto T., and Weissman I.L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404 (2000) 193-197
2. Kondo M., Weissman I.L., and Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91 (1997) 661-672
3. Rodewald H.R., Moingeon P., Lucich J.L., Dosiou C., Lopez P., and Reinherz E.L. A population of early fetal thymocytes expressing Fc gamma RII/III contains precursors of T lymphocytes and natural killer cells. Cell 69 (1992) 139-150
4. Carlyle J.R., Michie A.M., Furlonger C., Nakano T., Lenardo M.J., Paige C.J., and Zuniga-Pflucker J.C. Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med 186 (1997) 173-182
5. Ikawa T., Kawamoto H., Fujimoto S., and Katsura Y. Commitment of common T/Natural killer (NK) progenitors to unipotent T and NK progenitors in the murine fetal thymus revealed by a single progenitor assay. J Exp Med 190 (1999) 1617-1626
6. Yoshida H., Honda K., Shinkura R., Adachi S., Nishikawa S., Maki K., Ikuta K., and Nishikawa S.I. IL-7 receptor alpha+ CD3(-) cells in the embryonic intestine induces the organizing center of Peyer's patches. Int Immunol 11 (1999) 643-655
7. Finke D., Acha-Orbea H., Mattis A., Lipp M., and Kraehenbuhl J. CD4+CD3- cells induce Peyer's patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 17 (2002) 363-373
8. Kanamori Y., Ishimaru K., Nanno M., Maki K., Ikuta K., Nariuchi H., and Ishikawa H. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J Exp Med 184 (1996) 1449-1459
9. Yoshida H., Naito A., Inoue J., Satoh M., Santee-Cooper S.M., Ware C.F., Togawa A., Nishikawa S., and Nishikawa S. Different cytokines induce surface lymphotoxin-alphabeta on IL-7 receptor-alpha cells that differentially engender lymph nodes and Peyer's patches. Immunity 17 (2002) 823-833
10. Saito H., Kanamori Y., Takemori T., Nariuchi H., Kubota E., Takahashi-Iwanaga H., Iwanaga T., and Ishikawa H. Generation of intestinal T cells from progenitors residing in gut cryptopatches. Science 280 (1998) 275-278
11. Suzuki K., Oida T., Hamada H., Hitotsumatsu O., Watanabe M., Hibi T., Yamamoto H., Kubota E., Kaminogawa S., and Ishikawa H. Gut cryptopatches: direct evidence of extrathymic anatomical sites for intestinal T lymphopoiesis. Immunity 13 (2000) 691-702
12. Eberl G., and Littman D.R. Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+ cells. Science 305 (2004) 248-251
13. Howie D., Spencer J., DeLord D., Pitzalis C., Wathen N.C., Dogan A., Akbar A., and MacDonald T.T. Extrathymic T cell differentiation in the human intestine early in life. J Immunol 161 (1998) 5862-5872
14. Gunther U., Holloway J.A., Gordon J.N., Knight A., Chance V., Hanley N.A., Wilson D.I., French R., Spencer J., Steer H., Anderson G., and MacDonald T.T. Phenotypic characterization of CD3-7+ cells in developing human intestine and an analysis of their ability to differentiate into T cells. J Immunol 174 (2005) 5414-5422
15. Williams A.M., Bland P.W., Phillips A.C., Turner S., Brooklyn T., Shaya G., Spicer R.D., and Probert C.S. Intestinal alpha beta T cells differentiate and rearrange antigen receptor genes in situ in the human infant. J Immunol 173 (2004) 7190-7199
16. Bas A., Hammarstrom S.G., and Hammarstrom M.L. Extrathymic TCR gene rearrangement in human small intestine: identification of new splice forms of recombination activating gene-1 mRNA with selective tissue expression. J Immunol 171 (2003) 3359-3371
17. Ashman L.K., Cambareri A.C., To L.B., Levinsky R.J., and Juttner C.A. Expression of the YB5.B8 antigen (c-kit proto-oncogene product) in normal human bone marrow. Blood 78 (1991) 30-37
18. Res P., Martinez-Caceres E., Cristina Jaleco A., Staal F., Noteboom E., Weijer K., and Spits H. CD34+CD38dim cells in the human thymus can differentiate into T, natural killer, and dendritic cells but are distinct from pluripotent stem cells. Blood 87 (1996) 5196-5206
19. Sanchez M.J., Spits H., Lanier L.L., and Phillips J.H. Human natural killer cell committed thymocytes and their relation to the T cell lineage. J Exp Med 178 (1993) 1857-1866
20. Lennard-Jones J.E. Classification of inflammatory bowel disease. Scand J Gastroenterol Suppl 170 (1989) 2-6 16-19
21. Gower-Rousseau C., Salomez J.L., Dupas J.L., Marti R., Nuttens M.C., Votte A., Lemahieu M., Lemaire B., Colombel J.F., and Cortot A. Incidence of inflammatory bowel disease in northern France (1988-1990). Gut 35 (1994) 1433-1438
22. Bandeira A., Mota-Santos T., Itohara S., Degermann S., Heusser C., Tonegawa S., and Coutinho A. Localization of gamma/delta T cells to the intestinal epithelium is independent of normal microbial colonization. J Exp Med 172 (1990) 239-244
23. Ishikawa H., Li Y., Abeliovich A., Yamamoto S., Kaufmann S.H., and Tonegawa S. Cytotoxic and interferon gamma-producing activities of gamma delta T cells in the mouse intestinal epithelium are strain dependent. Proc Natl Acad Sci U S A 90 (1993) 8204-8208
24. Eldridge J.H., Kiyono H., Michalek S.M., and McGhee J.R. Evidence for a mature B cell subpopulation in Peyer's patches of young adult xid mice. J Exp Med 157 (1983) 789-794
25. Chang L., Gusewitch G.A., Chritton D.B., Folz J.C., Lebeck L.K., and Nehlsen-Cannarella S.L. Rapid flow cytometric assay for the assessment of natural killer cell activity. J Immunol Methods 166 (1993) 45-54
26. Horie K., Fujita J., Takakura K., Kanzaki H., Suginami H., Iwai M., Nakayama H., and Mori T. The expression of c-kit protein in human adult and fetal tissues. Hum Reprod 8 (1993) 1955-1962
27. Feyerabend T.B., Hausser H., Tietz A., Blum C., Hellman L., Straus A.H., Takahashi H.K., Morgan E.S., Dvorak A.M., Fehling H.J., and Rodewald H.R. Loss of histochemical identity in mast cells lacking carboxypeptidase A. Mol Cell Biol 25 (2005) 6199-6210
28. Civin C.I., Strauss L.C., Brovall C., Fackler M.J., Schwartz J.F., and Shaper J.H. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol 133 (1984) 157-165
29. Sanchez M.J., Muench M.O., Roncarolo M.G., Lanier L.L., and Phillips J.H. Identification of a common T/natural killer cell progenitor in human fetal thymus. J Exp Med 180 (1994) 569-576
30. Peiper S.C., Ashmun R.A., and Look A.T. Molecular cloning, expression, and chromosomal localization of a human gene encoding the CD33 myeloid differentiation antigen. Blood 72 (1988) 314-321
31. Miller J.S., Alley K.A., and McGlave P. Differentiation of natural killer (NK) cells from human primitive marrow progenitors in a stroma-based long-term culture system: identification of a CD34+7+ NK progenitor. Blood 83 (1994) 2594-2601
32. Kim S., Iizuka K., Kang H.S., Dokun A., French A.R., Greco S., and Yokoyama W.M. In vivo developmental stages in murine natural killer cell maturation. Nat Immunol 3 (2002) 523-528
33. Cepek K.L., Parker C.M., Madara J.L., and Brenner M.B. Integrin alpha E beta 7 mediates adhesion of T lymphocytes to epithelial cells. J Immunol 150 (1993) 3459-3470
34. Anderson M.K., Hernandez-Hoyos G., Diamond R.A., and Rothenberg E.V. Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126 (1999) 3131-3148
35. Scott E.W., Simon M.C., Anastasi J., and Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265 (1994) 1573-1577
36. Yokota Y., Mansouri A., Mori S., Sugawara S., Adachi S., Nishikawa S., and Gruss P. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397 (1999) 702-706
37. Iizuka K., Chaplin D.D., Wang Y., Wu Q., Pegg L.E., Yokoyama W.M., and Fu Y.X. Requirement for membrane lymphotoxin in natural killer cell development. Proc Natl Acad Sci U S A 96 (1999) 6336-6340
38. Alimzhanov M.B., Kuprash D.V., Kosco-Vilbois M.H., Luz A., Turetskaya R.L., Tarakhovsky A., Rajewsky K., Nedospasov S.A., and Pfeffer K. Abnormal development of secondary lymphoid tissues in lymphotoxin beta-deficient mice. Proc Natl Acad Sci U S A 94 (1997) 9302-9307
39. Hanna J., Gonen-Gross T., Fitchett J., Rowe T., Daniels M., Arnon T.I., Gazit R., Joseph A., Schjetne K.W., Steinle A., Porgador A., Mevorach D., Goldman-Wohl D., Yagel S., LaBarre M.J., Buckner J.H., and Mandelboim O. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest 114 (2004) 1612-1623
40. Colucci F., Caligiuri M.A., and Di Santo J.P. What does it take to make a natural killer?. Nat Rev Immunol 3 (2003) 413-425
41. Pang G., Buret A., Batey R.T., Chen Q.Y., Couch L., Cripps A., and Clancy R. Morphological, phenotypic and functional characteristics of a pure population of CD56+ CD16- CD3- large granular lymphocytes generated from human duodenal mucosa. Immunology 79 (1993) 498-505
42. Leon F., Roldan E., Sanchez L., Camarero C., Bootello A., and Roy G. Human small-intestinal epithelium contains functional natural killer lymphocytes. Gastroenterology 125 (2003) 345-356
43. Lanier L.L., Le A.M., Civin C.I., Loken M.R., and Phillips J.H. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol 136 (1986) 4480-4486
44. Cooper M.A., Fehniger T.A., Turner S.C., Chen K.S., Ghaheri B.A., Ghayur T., Carson W.E., and Caligiuri M.A. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97 (2001) 3146-3151
45. Campbell J.J., Qin S., Unutmaz D., Soler D., Murphy K.E., Hodge M.R., Wu L., and Butcher E.C. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J Immunol 166 (2001) 6477-6482
46. Robertson M.J. Role of chemokines in the biology of natural killer cells. J Leukoc Biol 71 (2002) 173-183
47. Podolsky D.K. Inflammatory bowel disease. N Engl J Med 347 (2002) 417-429
48. Di Santo J.P. Natural killer cell developmental pathways: a question of balance. Annu Rev Immunol 24 (2006) 257-286
49. Spits H., Blom B., Jaleco A.C., Weijer K., Verschuren M.C., van Dongen J.J., Heemskerk M.H., and Res P.C. Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol Rev 165 (1998) 75-86
50. Oida T., Suzuki K., Nanno M., Kanamori Y., Saito H., Kubota E., Kato S., Itoh M., Kaminogawa S., and Ishikawa H. Role of gut cryptopatches in early extrathymic maturation of intestinal intraepithelial T cells. J Immunol 164 (2000) 3616-3626
51. Mebius R.E., Rennert P., and Weissman I.L. Developing lymph nodes collect CD4+CD3- LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7 (1997) 493-504
52. Yoshida H., Kawamoto H., Santee S.M., Hashi H., Honda K., Nishikawa S., Ware C.F., Katsura Y., and Nishikawa S.I. Expression of alpha(4)beta(7) integrin defines a distinct pathway of lymphoid progenitors committed to T cells, fetal intestinal lymphotoxin producer, NK, and dendritic cells. J Immunol 167 (2001) 2511-2521
53. Fiocchi C., Tubbs R.R., and Youngman K.R. Human intestinal mucosal mononuclear cells exhibit lymphokine-activated killer cell activity. Gastroenterology 88 (1985) 625-637
54. Shibuya A., Nagayoshi K., Nakamura K., and Nakauchi H. Lymphokine requirement for the generation of natural killer cells from CD34+ hematopoietic progenitor cells. Blood 85 (1995) 3538-3546
55. Handgretinger R., Schafer H.J., Baur F., Frank D., Ottenlinger C., Buhring H.J., and Niethammer D. Expression of an early myelopoietic antigen (CD33) on a subset of human umbilical cord blood-derived natural killer cells. Immunol Lett 37 (1993) 223-228
56. Freud A.G., Becknell B., Roychowdhury S., Mao H.C., Ferketich A.K., Nuovo G.J., Hughes T.L., Marburger T.B., Sung J., Baiocchi R.A., Guimond M., and Caligiuri M.A. A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 22 (2005) 295-304
57. Keilbaugh S.A., Shin M.E., Banchereau R.F., McVay L.D., Boyko N., Artis D., Cebra J.J., and Wu G.D. Activation of RegIIIbeta/gamma and interferon gamma expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut. Gut 54 (2005) 623-629
58. Dalbeth N., Gundle R., Davies R.J., Lee Y.C., McMichael A.J., and Callan M.F. CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J Immunol 173 (2004) 6418-6426
59. Yang L., Dybedal I., Bryder D., Nilsson L., Sitnicka E., Sasaki Y., and Jacobsen S.E. IFN-gamma negatively modulates self-renewal of repopulating human hemopoietic stem cells. J Immunol 174 (2005) 752-757