β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response: Immunity

C. Brakebusch; S. Fillatreau; A.J. Potocnik; G. Bungartz; P. Wilhelm; M. Svensson; P. Kearney; H. Körner; D. Gray; R. Fässler

doi:10.1016/S1074-7613(02)00281-9

β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response: Immunity

C. Brakebusch, S. Fillatreau, A.J. Potocnik, G. Bungartz, P. Wilhelm, M. Svensson, P. Kearney, H. Körner, D. Gray, R. Fässler

School of Biological Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Several experimental evidences suggested that β1 integrin-mediated adhesion of hematopoietic stem cells (HSC) is important for their function in the bone marrow (BM). Using induced deletion of the β1 integrin gene restricted to the hematopoietic system, we show that β1 integrin is not essential for HSC retention in the BM, hematopoiesis, and trafficking of lymphocytes. However, immunization with a T cell-dependent antigen resulted in virtually no IgM production and an increased secretion of IgG in mutant mice, while the response to a T cell-independent type 2 antigen showed decreases in both IgM and IgG. These data suggest that β1 integrins are necessary for the primary IgM antibody response.

Original language	English
Pages (from-to)	465-477
Number of pages	13
Journal	Immunity
Volume	16
Issue number	3
DOIs	https://doi.org/10.1016/S1074-7613(02)00281-9
Publication status	Published - 2002

Keywords

beta1 integrin
immunoglobulin G
immunoglobulin M antibody
immunoglobulin M
animal cell
animal experiment
antibody response
article
bone marrow
cell adhesion
controlled study
hematopoiesis
hematopoietic stem cell
immunization
immunoglobulin production
mouse
nonhuman
priority journal
T lymphocyte
animal
antibody production
B lymphocyte
biosynthesis
gene deletion
gene expression regulation
genetics
immunology
Animals
Antibody Formation
Antigens, CD29
B-Lymphocytes
Gene Deletion
Gene Expression Regulation
Hematopoiesis
Immunoglobulin M
Mice
T-Lymphocytes

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10.1016/S1074-7613(02)00281-9

http://www.scopus.com/inward/record.url?eid=2-s2.0-18344384036&partnerID=40&md5=6b1bef247206b6521d72bc3e25daa6ec

Cite this

@article{7699654e680141f682baab4d037e963e,

title = "β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response: Immunity",

abstract = "Several experimental evidences suggested that β1 integrin-mediated adhesion of hematopoietic stem cells (HSC) is important for their function in the bone marrow (BM). Using induced deletion of the β1 integrin gene restricted to the hematopoietic system, we show that β1 integrin is not essential for HSC retention in the BM, hematopoiesis, and trafficking of lymphocytes. However, immunization with a T cell-dependent antigen resulted in virtually no IgM production and an increased secretion of IgG in mutant mice, while the response to a T cell-independent type 2 antigen showed decreases in both IgM and IgG. These data suggest that β1 integrins are necessary for the primary IgM antibody response.",

keywords = "beta1 integrin, immunoglobulin G, immunoglobulin M antibody, immunoglobulin M, animal cell, animal experiment, antibody response, article, bone marrow, cell adhesion, controlled study, hematopoiesis, hematopoietic stem cell, immunization, immunoglobulin production, mouse, nonhuman, priority journal, T lymphocyte, animal, antibody production, B lymphocyte, biosynthesis, gene deletion, gene expression regulation, genetics, immunology, Animals, Antibody Formation, Antigens, CD29, B-Lymphocytes, Gene Deletion, Gene Expression Regulation, Hematopoiesis, Immunoglobulin M, Mice, T-Lymphocytes",

author = "C. Brakebusch and S. Fillatreau and A.J. Potocnik and G. Bungartz and P. Wilhelm and M. Svensson and P. Kearney and H. K{\"o}rner and D. Gray and R. F{\"a}ssler",

note = "Cited By :49 Export Date: 11 March 2015 CODEN: IUNIE Correspondence Address: Brakebusch, C.; Lund University, 22185 Lund, Sweden; email: brakebus@biochem.mpg.de Chemicals/CAS: Antigens, CD29; Immunoglobulin M References: Agenes, F., Rosado, M.M., Freitas, A.A., Considerations on B cell homeostasis (2000) Curr. Top. Microbiol. Immunol., 252, pp. 68-75; Arroyo, A.G., Yang, J.T., Rayburn, H., Hynes, R.O., Differential requirements for α4 integrins during fetal and adult hematopoiesis (1996) Cell, 85, pp. 997-1008; Arroyo, A.G., Yang, J.T., Rayburn, H., Hynes, R.O., α4 integrins regulate the proliferation/differentiation balance of multilineage hematopoietic progenitors in vivo (1999) Immunity, 11, pp. 555-566; Arroyo, A.G., Taverna, D., Whittaker, C.A., Strauch, U.G., Bader, B.L., Rayburn, H., Crowley, D., Hynes, R.O., In vivo roles of integrins during leukocyte development and traffic: Insights from the analysis of mice chimeric for α5, αv, and α4 integrins (2000) J. Immunol., 165, pp. 4667-4675; Blystone, S.D., Slater, S.E., Williams, M.P., Crow, M.T., Brown, E.J., A molecular mechanism of integrin crosstalk: αvβ3 suppression of calcium/calmodulin-dependent protein kinase II regulates α5β1 function (1999) J. Cell Biol., 145, pp. 889-897; Coligan, J.E., Kruisbeek, A.M., Margulies, D.H., Shevach, E., Strober, W., (1995) Current Protocols in Immunology, , Wiley and Sons, Inc; Crisa, L., Cirulli, V., Ellisman, M.H., Ishii, J.K., Elices, M.J., Salomon, D.R., Cell adhesion and migration are regulated at distinct stages of thymic T cell development: The roles of fibronectin, VLA4, and VLA5 (1996) J. Exp. Med., 184, pp. 215-228; Damle, N.K., Aruffo, A., Vascular cell adhesion molecule 1 induces T-cell antigen receptor-dependent activation of CD4+T lymphocytes (1991) Proc. Natl. Acad. Sci. USA, 88, pp. 6403-6407; Engelhardt, B., Laschinger, M., Schulz, M., Samulowitz, U., Vestweber, D., Hoch, G., The development of experimental autoimmune encephalomyelitis in the mouse requires α4-integrin but not α4β7-integrin (1998) J. Clin. Invest., 102, pp. 2096-2105; F{\"a}ssler, R., Meyer, M., Consequences of lack of β1 integrin gene expression in mice (1995) Genes Dev., 9, pp. 1896-1908; F{\"o}rster, R., Mattis, A.E., Kremmer, E., Wolf, E., Brem, G., Lipp, M., A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen (1996) Cell, 87, pp. 1037-1047; F{\"o}rster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-M{\"u}ller, I., Wolf, E., Lipp, M., CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs (1999) Cell, 99, pp. 23-33; Friedl, P., Brocker, E.B., T cell migration in three-dimensional extracellular matrix: Guidance by polarity and sensations (2000) Dev. Immunol., 7, pp. 249-266; Garcia de Vinuesa, C., O'Leary, P., Sze, D.M., Toellner, K.M., MacLennan, I.C., T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci (1999) Eur. J. Immunol., 29, pp. 1314-1323; Giancotti, F.G., Ruoslahti, E., Integrin signaling (1999) Science, 285, pp. 1028-1032; Gonzalez-Amaro, R., Sanchez-Madrid, F., Cell adhesion molecules: Selectins and integrins (1999) Crit. Rev. Immunol., 19, pp. 389-429; Gray, D., Dullforce, P., Jainandunsing, S., Memory B cell development but not germinal centre formation is impaired by in vivo blockade of CD40-CD40 ligand interaction (1994) J. Exp. Med., 180, pp. 141-155; Groux, H., Huet, S., Valentin, H., Pham, D., Bernard, A., Suppressor effects and cyclic AMP accumulation by the CD29 molecule of CD4+ lymphocytes (1989) Nature, 339, pp. 152-154; Gulbranson-Judge, A., Tybulewicz, V.L., Walters, A.E., Toellner, K.M., MacLennan, I.C., Turner, M., Defective immunoglobulin class switching in Vav-deficient mice is attributable to compromised T cell help (1999) Eur. J. Immunol., 29, pp. 477-487; Hirsch, E., Iglesias, A., Potocnik, A.J., Hartmann, U., F{\"a}ssler, R., Impaired migration but not differentiation of haematopoietic stem cells in the absence of β1 integrins (1996) Nature, 380, pp. 171-175; Hogg, N., Bates, P.A., Genetic analysis of integrin function in man: LAD-1 and other syndromes (2000) Matrix Biol., 19, pp. 211-222; Hurley, R.W., McCarthy, J.B., Verfaillie, C.M., Direct adhesion to BM stroma via fibronectin receptors inhibits hematopoietic progenitor proliferation (1995) J. Clin. Invest., 96, pp. 511-519; Hynes, R.O., Integrins: Versatility, modulation, and signaling in cell adhesion (1992) Cell, 69, pp. 11-25; Jacob, J., Kelsoe, G., In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers (1992) J. Exp. Med., 176, pp. 679-687; Jenkinson, E.J., Franchi, L.L., Kingston, R., Owen, J.J., Effect of deoxyguanosine on lymphopoiesis in the developing thymus rudiment in vitro: Application in the production of chimeric thymus rudiments (1982) Eur. J. Immunol., 12, pp. 583-587; Kawabe, T., Naka, T., Yoshida, K., Tanaka, T., Fujiwara, H., Suematsu, S., Yoshida, N., Kikutani, H., The immune responses in CD40-deficient mice: Impaired immunoglobulin class switching and germinal center formation (1994) Immunity, 1, pp. 167-178; Kim, U., Qin, X.F., Gong, S., Stevens, S., Luo, Y., Nussenzweig, M., Roeder, R.G., The B-cell-specific transcription coactivator OCA-B/OBF-1/Bob-1 is essential for normal production of immunoglobulin isotypes (1996) Nature, 383, pp. 542-547; K{\"o}rner, H., Cretney, E., Wilhelm, P., Kelly, J.M., Rollinghoff, M., Sedgwick, J.D., Smyth, M.J., Tumor necrosis factor sustains the generalized lymphoproliferative disorder (gld) phenotype (2000) J. Exp. Med., 191, pp. 89-96; K{\"u}hn, R., Schwenk, F., Aguet, M., Rajewsky, K., Inducible gene targeting in mice (1995) Science, 269, pp. 1427-1429; Kupiec-Weglinski, J.W., De Sousa, M., Lymphocyte traffic is modified in vivo by anti-laminin antibody (1991) Immunology, 72, pp. 312-313; Lehnert, K., Print, C.G., Yang, Y., Krissansen, G.W., MAdCAM-1 costimulates T cell proliferation exclusively through integrin α4β7, whereas VCAM-1 and CS-1peptide use α4β1: Evidence for {"}remote{"} costimulation and induction of hyperresponsiveness to B7 molecules (1998) Eur. J. Immunol., 28, pp. 3605-3615; Liu, Y.-J., Lane, P.J.L., Chan, E.Y.-T., MacLennan, I.C.M., Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens (1992) Eur. J. 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year = "2002",

doi = "10.1016/S1074-7613(02)00281-9",

language = "English",

volume = "16",

pages = "465--477",

journal = "Immunity",

issn = "1074-7613",

publisher = "Cell Press",

number = "3",

}

β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response : Immunity. / Brakebusch, C.; Fillatreau, S.; Potocnik, A.J.; Bungartz, G.; Wilhelm, P.; Svensson, M.; Kearney, P.; Körner, H.; Gray, D.; Fässler, R.

In: Immunity, Vol. 16, No. 3, 2002, p. 465-477.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response

T2 - Immunity

AU - Brakebusch, C.

AU - Fillatreau, S.

AU - Potocnik, A.J.

AU - Bungartz, G.

AU - Wilhelm, P.

AU - Svensson, M.

AU - Kearney, P.

AU - Körner, H.

AU - Gray, D.

AU - Fässler, R.

N1 - Cited By :49 Export Date: 11 March 2015 CODEN: IUNIE Correspondence Address: Brakebusch, C.; Lund University, 22185 Lund, Sweden; email: brakebus@biochem.mpg.de Chemicals/CAS: Antigens, CD29; Immunoglobulin M References: Agenes, F., Rosado, M.M., Freitas, A.A., Considerations on B cell homeostasis (2000) Curr. Top. Microbiol. Immunol., 252, pp. 68-75; Arroyo, A.G., Yang, J.T., Rayburn, H., Hynes, R.O., Differential requirements for α4 integrins during fetal and adult hematopoiesis (1996) Cell, 85, pp. 997-1008; Arroyo, A.G., Yang, J.T., Rayburn, H., Hynes, R.O., α4 integrins regulate the proliferation/differentiation balance of multilineage hematopoietic progenitors in vivo (1999) Immunity, 11, pp. 555-566; Arroyo, A.G., Taverna, D., Whittaker, C.A., Strauch, U.G., Bader, B.L., Rayburn, H., Crowley, D., Hynes, R.O., In vivo roles of integrins during leukocyte development and traffic: Insights from the analysis of mice chimeric for α5, αv, and α4 integrins (2000) J. Immunol., 165, pp. 4667-4675; Blystone, S.D., Slater, S.E., Williams, M.P., Crow, M.T., Brown, E.J., A molecular mechanism of integrin crosstalk: αvβ3 suppression of calcium/calmodulin-dependent protein kinase II regulates α5β1 function (1999) J. Cell Biol., 145, pp. 889-897; Coligan, J.E., Kruisbeek, A.M., Margulies, D.H., Shevach, E., Strober, W., (1995) Current Protocols in Immunology, , Wiley and Sons, Inc; Crisa, L., Cirulli, V., Ellisman, M.H., Ishii, J.K., Elices, M.J., Salomon, D.R., Cell adhesion and migration are regulated at distinct stages of thymic T cell development: The roles of fibronectin, VLA4, and VLA5 (1996) J. Exp. Med., 184, pp. 215-228; Damle, N.K., Aruffo, A., Vascular cell adhesion molecule 1 induces T-cell antigen receptor-dependent activation of CD4+T lymphocytes (1991) Proc. Natl. Acad. Sci. USA, 88, pp. 6403-6407; Engelhardt, B., Laschinger, M., Schulz, M., Samulowitz, U., Vestweber, D., Hoch, G., The development of experimental autoimmune encephalomyelitis in the mouse requires α4-integrin but not α4β7-integrin (1998) J. Clin. Invest., 102, pp. 2096-2105; Fässler, R., Meyer, M., Consequences of lack of β1 integrin gene expression in mice (1995) Genes Dev., 9, pp. 1896-1908; Förster, R., Mattis, A.E., Kremmer, E., Wolf, E., Brem, G., Lipp, M., A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen (1996) Cell, 87, pp. 1037-1047; Förster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Müller, I., Wolf, E., Lipp, M., CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs (1999) Cell, 99, pp. 23-33; Friedl, P., Brocker, E.B., T cell migration in three-dimensional extracellular matrix: Guidance by polarity and sensations (2000) Dev. Immunol., 7, pp. 249-266; Garcia de Vinuesa, C., O'Leary, P., Sze, D.M., Toellner, K.M., MacLennan, I.C., T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci (1999) Eur. J. Immunol., 29, pp. 1314-1323; Giancotti, F.G., Ruoslahti, E., Integrin signaling (1999) Science, 285, pp. 1028-1032; Gonzalez-Amaro, R., Sanchez-Madrid, F., Cell adhesion molecules: Selectins and integrins (1999) Crit. Rev. Immunol., 19, pp. 389-429; Gray, D., Dullforce, P., Jainandunsing, S., Memory B cell development but not germinal centre formation is impaired by in vivo blockade of CD40-CD40 ligand interaction (1994) J. Exp. Med., 180, pp. 141-155; Groux, H., Huet, S., Valentin, H., Pham, D., Bernard, A., Suppressor effects and cyclic AMP accumulation by the CD29 molecule of CD4+ lymphocytes (1989) Nature, 339, pp. 152-154; Gulbranson-Judge, A., Tybulewicz, V.L., Walters, A.E., Toellner, K.M., MacLennan, I.C., Turner, M., Defective immunoglobulin class switching in Vav-deficient mice is attributable to compromised T cell help (1999) Eur. J. Immunol., 29, pp. 477-487; Hirsch, E., Iglesias, A., Potocnik, A.J., Hartmann, U., Fässler, R., Impaired migration but not differentiation of haematopoietic stem cells in the absence of β1 integrins (1996) Nature, 380, pp. 171-175; Hogg, N., Bates, P.A., Genetic analysis of integrin function in man: LAD-1 and other syndromes (2000) Matrix Biol., 19, pp. 211-222; Hurley, R.W., McCarthy, J.B., Verfaillie, C.M., Direct adhesion to BM stroma via fibronectin receptors inhibits hematopoietic progenitor proliferation (1995) J. Clin. Invest., 96, pp. 511-519; Hynes, R.O., Integrins: Versatility, modulation, and signaling in cell adhesion (1992) Cell, 69, pp. 11-25; Jacob, J., Kelsoe, G., In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers (1992) J. Exp. Med., 176, pp. 679-687; Jenkinson, E.J., Franchi, L.L., Kingston, R., Owen, J.J., Effect of deoxyguanosine on lymphopoiesis in the developing thymus rudiment in vitro: Application in the production of chimeric thymus rudiments (1982) Eur. J. 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PY - 2002

Y1 - 2002

N2 - Several experimental evidences suggested that β1 integrin-mediated adhesion of hematopoietic stem cells (HSC) is important for their function in the bone marrow (BM). Using induced deletion of the β1 integrin gene restricted to the hematopoietic system, we show that β1 integrin is not essential for HSC retention in the BM, hematopoiesis, and trafficking of lymphocytes. However, immunization with a T cell-dependent antigen resulted in virtually no IgM production and an increased secretion of IgG in mutant mice, while the response to a T cell-independent type 2 antigen showed decreases in both IgM and IgG. These data suggest that β1 integrins are necessary for the primary IgM antibody response.

AB - Several experimental evidences suggested that β1 integrin-mediated adhesion of hematopoietic stem cells (HSC) is important for their function in the bone marrow (BM). Using induced deletion of the β1 integrin gene restricted to the hematopoietic system, we show that β1 integrin is not essential for HSC retention in the BM, hematopoiesis, and trafficking of lymphocytes. However, immunization with a T cell-dependent antigen resulted in virtually no IgM production and an increased secretion of IgG in mutant mice, while the response to a T cell-independent type 2 antigen showed decreases in both IgM and IgG. These data suggest that β1 integrins are necessary for the primary IgM antibody response.

KW - beta1 integrin

KW - immunoglobulin G

KW - immunoglobulin M antibody

KW - immunoglobulin M

KW - animal cell

KW - animal experiment

KW - antibody response

KW - article

KW - bone marrow

KW - cell adhesion

KW - controlled study

KW - hematopoiesis

KW - hematopoietic stem cell

KW - immunization

KW - immunoglobulin production

KW - mouse

KW - nonhuman

KW - priority journal

KW - T lymphocyte

KW - animal

KW - antibody production

KW - B lymphocyte

KW - biosynthesis

KW - gene deletion

KW - gene expression regulation

KW - genetics

KW - immunology

KW - Animals

KW - Antibody Formation

KW - Antigens, CD29

KW - B-Lymphocytes

KW - Gene Deletion

KW - Gene Expression Regulation

KW - Hematopoiesis

KW - Immunoglobulin M

KW - Mice

KW - T-Lymphocytes

U2 - 10.1016/S1074-7613(02)00281-9

DO - 10.1016/S1074-7613(02)00281-9

M3 - Article

VL - 16

SP - 465

EP - 477

JO - Immunity

JF - Immunity

SN - 1074-7613

IS - 3

ER -

β1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response: Immunity

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