Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo

Research output: Contribution to journalJournal articleResearchpeer-review

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Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo. / Janssens, Rik; Mortier, Anneleen; Boff, Daiane; Vanheule, Vincent; Gouwy, Mieke; Franck, Charlotte; Larsen, Olav; Rosenkilde, Mette M.; Damme, Jo Van; Amaral, Flávio A.; Teixeira, Mauro M.; Struyf, Sofie; Proost, Paul.

In: OncoTarget, Vol. 7, No. 38, 2016, p. 62439-62459.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Janssens, R, Mortier, A, Boff, D, Vanheule, V, Gouwy, M, Franck, C, Larsen, O, Rosenkilde, MM, Damme, JV, Amaral, FA, Teixeira, MM, Struyf, S & Proost, P 2016, 'Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo', OncoTarget, vol. 7, no. 38, pp. 62439-62459. https://doi.org/10.18632/oncotarget.11516

APA

Janssens, R., Mortier, A., Boff, D., Vanheule, V., Gouwy, M., Franck, C., Larsen, O., Rosenkilde, M. M., Damme, J. V., Amaral, F. A., Teixeira, M. M., Struyf, S., & Proost, P. (2016). Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo. OncoTarget, 7(38), 62439-62459. https://doi.org/10.18632/oncotarget.11516

Vancouver

Janssens R, Mortier A, Boff D, Vanheule V, Gouwy M, Franck C et al. Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo. OncoTarget. 2016;7(38):62439-62459. https://doi.org/10.18632/oncotarget.11516

Author

Janssens, Rik ; Mortier, Anneleen ; Boff, Daiane ; Vanheule, Vincent ; Gouwy, Mieke ; Franck, Charlotte ; Larsen, Olav ; Rosenkilde, Mette M. ; Damme, Jo Van ; Amaral, Flávio A. ; Teixeira, Mauro M. ; Struyf, Sofie ; Proost, Paul. / Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo. In: OncoTarget. 2016 ; Vol. 7, No. 38. pp. 62439-62459.

Bibtex

@article{3047ff13ecaa41178a82fd5dbc22809c,
title = "Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo",
abstract = "The chemokine CXCL12/stromal cell-derived factor-1 is important for leukocyte migration to lymphoid organs and inflamed tissues and stimulates tumor development. In vitro, CXCL12 activity through CXCR4 is abolished by proteolytic processing. However, limited information is available on in vivo effects of posttranslationally modified CXCL12. Natural CXCL12 was purified from the coculture supernatant of stromal cells stimulated with leukocytes and inflammatory agents. In this conditioned medium, CXCL12 with a nitration on Tyr7, designated [3-NT7]CXCL12, was discovered via Edman degradation. CXCL12 and [3-NT7]CXCL12 were chemically synthesized to evaluate the biological effects of this modification. [3-NT7]CXCL12 recruited β-arrestin 2 and phosphorylated the Akt kinase similar to CXCL12 in receptor-transfected cells. Also the affinity of CXCL12 and [3-NT7]CXCL12 for glycosaminoglycans, the G protein-coupled chemokine receptor CXCR4 and the atypical chemokine receptor ACKR3 were comparable. However, [3-NT7]CXCL12 showed a reduced ability to enhance intracellular calcium concentrations, to generate inositol triphosphate, to phosphorylate ERK1/2 and to induce monocyte and lymphocyte chemotaxis in vitro. Moreover, nitrated CXCL12 failed to induce in vivo extravasation of lymphocytes to the joint. In summary, nitration on Tyr7 under inflammatory conditions is a novel natural posttranslational regulatory mechanism of CXCL12 which may downregulate the CXCR4-mediated inflammatory and tumor-promoting activities of CXCL12.",
keywords = "Chemokine, Chemotaxis, Extravasation, Lymphocyte migration, Posttranslational modification",
author = "Rik Janssens and Anneleen Mortier and Daiane Boff and Vincent Vanheule and Mieke Gouwy and Charlotte Franck and Olav Larsen and Rosenkilde, {Mette M.} and Damme, {Jo Van} and Amaral, {Fl{\'a}vio A.} and Teixeira, {Mauro M.} and Sofie Struyf and Paul Proost",
year = "2016",
doi = "10.18632/oncotarget.11516",
language = "English",
volume = "7",
pages = "62439--62459",
journal = "Oncotarget",
issn = "1949-2553",
publisher = "Impact Journals LLC",
number = "38",

}

RIS

TY - JOUR

T1 - Natural nitration of CXCL12 reduces its signaling capacity and chemotactic activity in vitro and abrogates intra-articular lymphocyte recruitment in vivo

AU - Janssens, Rik

AU - Mortier, Anneleen

AU - Boff, Daiane

AU - Vanheule, Vincent

AU - Gouwy, Mieke

AU - Franck, Charlotte

AU - Larsen, Olav

AU - Rosenkilde, Mette M.

AU - Damme, Jo Van

AU - Amaral, Flávio A.

AU - Teixeira, Mauro M.

AU - Struyf, Sofie

AU - Proost, Paul

PY - 2016

Y1 - 2016

N2 - The chemokine CXCL12/stromal cell-derived factor-1 is important for leukocyte migration to lymphoid organs and inflamed tissues and stimulates tumor development. In vitro, CXCL12 activity through CXCR4 is abolished by proteolytic processing. However, limited information is available on in vivo effects of posttranslationally modified CXCL12. Natural CXCL12 was purified from the coculture supernatant of stromal cells stimulated with leukocytes and inflammatory agents. In this conditioned medium, CXCL12 with a nitration on Tyr7, designated [3-NT7]CXCL12, was discovered via Edman degradation. CXCL12 and [3-NT7]CXCL12 were chemically synthesized to evaluate the biological effects of this modification. [3-NT7]CXCL12 recruited β-arrestin 2 and phosphorylated the Akt kinase similar to CXCL12 in receptor-transfected cells. Also the affinity of CXCL12 and [3-NT7]CXCL12 for glycosaminoglycans, the G protein-coupled chemokine receptor CXCR4 and the atypical chemokine receptor ACKR3 were comparable. However, [3-NT7]CXCL12 showed a reduced ability to enhance intracellular calcium concentrations, to generate inositol triphosphate, to phosphorylate ERK1/2 and to induce monocyte and lymphocyte chemotaxis in vitro. Moreover, nitrated CXCL12 failed to induce in vivo extravasation of lymphocytes to the joint. In summary, nitration on Tyr7 under inflammatory conditions is a novel natural posttranslational regulatory mechanism of CXCL12 which may downregulate the CXCR4-mediated inflammatory and tumor-promoting activities of CXCL12.

AB - The chemokine CXCL12/stromal cell-derived factor-1 is important for leukocyte migration to lymphoid organs and inflamed tissues and stimulates tumor development. In vitro, CXCL12 activity through CXCR4 is abolished by proteolytic processing. However, limited information is available on in vivo effects of posttranslationally modified CXCL12. Natural CXCL12 was purified from the coculture supernatant of stromal cells stimulated with leukocytes and inflammatory agents. In this conditioned medium, CXCL12 with a nitration on Tyr7, designated [3-NT7]CXCL12, was discovered via Edman degradation. CXCL12 and [3-NT7]CXCL12 were chemically synthesized to evaluate the biological effects of this modification. [3-NT7]CXCL12 recruited β-arrestin 2 and phosphorylated the Akt kinase similar to CXCL12 in receptor-transfected cells. Also the affinity of CXCL12 and [3-NT7]CXCL12 for glycosaminoglycans, the G protein-coupled chemokine receptor CXCR4 and the atypical chemokine receptor ACKR3 were comparable. However, [3-NT7]CXCL12 showed a reduced ability to enhance intracellular calcium concentrations, to generate inositol triphosphate, to phosphorylate ERK1/2 and to induce monocyte and lymphocyte chemotaxis in vitro. Moreover, nitrated CXCL12 failed to induce in vivo extravasation of lymphocytes to the joint. In summary, nitration on Tyr7 under inflammatory conditions is a novel natural posttranslational regulatory mechanism of CXCL12 which may downregulate the CXCR4-mediated inflammatory and tumor-promoting activities of CXCL12.

KW - Chemokine

KW - Chemotaxis

KW - Extravasation

KW - Lymphocyte migration

KW - Posttranslational modification

U2 - 10.18632/oncotarget.11516

DO - 10.18632/oncotarget.11516

M3 - Journal article

C2 - 27566567

AN - SCOPUS:84991824703

VL - 7

SP - 62439

EP - 62459

JO - Oncotarget

JF - Oncotarget

SN - 1949-2553

IS - 38

ER -

ID: 168855832