Difference between sentinel and non-sentinel lymph nodes in the distribution of dendritic cells and macrophages: An immunohistochemical and morphometric study using gastric regional nodes obtained in sentinel node navigation surgery for early gastric cancer.
CD169
DC‐SIGN
dendritic cells
gastric cancer
macrophages
morphometry
sentinel lymph node
Journal
Journal of anatomy
ISSN: 1469-7580
Titre abrégé: J Anat
Pays: England
ID NLM: 0137162
Informations de publication
Date de publication:
05 Oct 2024
05 Oct 2024
Historique:
revised:
16
09
2024
received:
22
04
2024
accepted:
16
09
2024
medline:
5
10
2024
pubmed:
5
10
2024
entrez:
5
10
2024
Statut:
aheadofprint
Résumé
The sentinel lymph node (SN) concept has a significant impact on cancer surgery. We aimed to examine which morphology of dendritic cells (DCs) and macrophages corresponds to "preconditioning" of the SN against cancer. Although macrophages are generally able to tolerate cancer metastasis, the CD169-positive subtype is believed to be a limited exception. Immunohistochemical and morphometric analyses were performed to examine DC-SIGN-, CD68-, and CD169-positive cells in SNs and non-SNs of 23 patients with gastric cancer with or without nodal metastasis. All patients survived for >5 years without recurrence. DCs were present in the subcapsular, paracortical, and medullary sinuses, the endothelia of which expressed DC-SIGN and smooth muscle actin (SMA). In the non-SNs of patients without metastasis, subcapsular DCs occupied a larger area than SNs, and this difference was statistically significant. Conversely, subcapsular DCs were likely to have migrated to the paracortical area of the SNs. DC clusters often overlapped with macrophage clusters; however, histiocytosis-like clusters of CD169-negative macrophages showed a smaller overlap. We found a significantly larger overlap between DC-SIGN and CD169-positive clusters in SNs than in non-SNs; the larger overlap seemed to correspond to a higher cross-presentation of cancer antigens between these cell populations. DC-SIGN-CD169-double positive cells might exist within this overlap. SNs in gastric cancers are usually preconditioned as a frontier of cancer immunity, but they may sometimes be suppressed earlier than non-SNs. DC-SIGN- and CD169-positive cells appeared to decrease owing to a long lag time from the primary lesion occurrence and a short distance from the metastasis.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.
Références
Angel, C.E., Chen, C.J.J., Horlacher, O.C., Winkler, S., John, T., Browning, J. et al. (2009) Distinctive localization of antigen‐presenting cells in human lymph nodes. Blood, 113, 1257–1267.
Aoki, M., Jin, Z.W., Ueda, K., Kamimura, G., Takeda‐Harada, A., Murakami, G. et al. (2023) Localization of macrophages and dendritic cells in human thoracic lymph node: An immunohistochemical study using surgically‐obtained specimens. Journal of Anatomy, 243(3), 504–516.
Botella‐Estrada, R., Dasi, F., Ramos, D., Nagore, E., Herrero, M., Gimenez, J. et al. (2005) Cytokine expression and dendritic cell density in melanoma sentinel node. Melanoma Research, 15, 99–106.
Chen, X., Zheng, Y., Liu, S., Yu, W. & Liu, Z. (2022) CD169+ subcapsular sinus macrophage‐derived microvesicles are associated with light zone follicular dendritic cells. European Journal of Immunology, 52, 1581–1594.
Cheong, C., Matos, I., Choi, J.H., Dandamudi, D.B., Shrestha, E., Longhi, M.P. et al. (2010) Microbial stimulation fully differentiates monocytes to DC‐ SIGN/CD209(+) dendritic cells for immune T cell areas. Cell, 143, 416–429.
Cochran, A.J., Huang, R.R., Lee, J., Itakura, E., Leong, S.P. & Essner, R. (2006) Tumor‐induced immune modulation of sentinel nodes. Nature Reviews Immunology, 6, 659–670.
Cochran, A.J., Morton, D.L., Stern, S., Lana, A.M., Essner, R. & Wen, D.R. (2001) Sentinel lymph nodes show profound downregulation of antigen‐presenting cells of the paracortex: implication for tumor biology and treatment. Modern Pathology, 14, 604–608.
Engering, A., van Vliet, S., Hebeda, K., Jackson, D.G., Prevo, R., Singh, S.K. et al. (2004) Dynamic populations of dendritic cell‐specific ICAM‐3 grabbing nonintegrin‐positive immature dendritic cells and liver/lymph node‐specific ICAM‐3 grabbing nonintegrin‐positive endothelial cells in the outer zones of the paracortex of human lymph nodes. The American Journal of Pathology, 164, 1587–1595.
Grabowska, J., Lopez‐Venegas, M.A., Affandi, A.J. & den Haan, J.M.M. (2018) CD169+ macrophages capture and dendritic cell instruct: the interplay of the gatekeeper and the general of the immune system. Frontiers in Immunology, 9, 2472. Available from: https://doi.org/10.3389/fimmu.2018.02472
Granelli‐Piperno, A., Pritsker, A., Pack, M., Shimeliovich, I., Arrighi, J.F., Park, C.G. et al. (2005) Dendritic cell‐specific intercellular adhesion molecule 3‐grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. Journal of Immunology, 175, 4265–4273.
Heeren, A.M., Rotman, J., Samuels, S., Zijlmans, H.J.M.A.A., Fons, G., van de Vijver, K.K. et al. (2021) Immune landscape in vulvar cancer‐draining lymph nodes indicates distinct immune escape mechanisms in support of metastatic spread and growth. J Immunother Cancer, 9, e003623.
Ito, M., Minamiya, Y., Kawai, H., Saito, S., Saito, H., Nakagawa, T. et al. (2006) Tumor‐derived TGFbeta‐1 induces dendritic cell apoptosis in the sentinel lymph node. Journal of Immunology, 176, 5637–5643.
Japanese Gastric cancer Association. (2011) Japanese classification of gastric carcinoma. Gastric Cancer, 14, 101–112.
Johnson, L.A. & Jackson, D.G. (2010) Inflammation‐induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin‐mediated dendritic cell transmigration. International Immunology, 22, 839–849.
Kamiya, S., Takeuchi, H., Fukuda, K., Kawakubo, H., Takahashi, N., Mitsumori, N. et al. (2021) A multicenter non‐randomized phase III study of sentinel node navigation surgery for early gastric cancer. The Japanese Journal of Clinical Oncology, 51, 305–309.
Kawasaki, N., Vela, J.L., Nycholat, C.M., Rademacher, C., Khurana, A., van Rooijen, N. et al. (2013) Targeted delivery of lipid‐antigen to macrophages via the CD169/sialoadhesin endocytic pathway induces robust invariant killer T cell activation. Proceedings of the National Academy of Sciences of the United States of America, 110, 7826–7831.
Kitagawa, Y., Fujii, H., Mukai, M., Kubota, T., Ando, N., Watanabe, M. et al. (2020) The role of the sentinel lymph node in gastrointestinal cancer. The Surgical Clinics of North America, 80, 1799–1809.
Kumamoto, K., Tasaki, T., Ohnishi, K., Shibata, M., Shimajiri, S., Harada, M. et al. (2021) CD169 expression on lymph node macrophages predicts in patients with gastric cancer. Front Oncologia, 11, 636751.
Lai, W.K., Sun, P.J., Zhang, J., Jennings, A., Lalor, P.F., Hubscher, S. et al. (2006) Expression of DC‐SIGN and DC‐SIGNR on human sinusoidal endothelium. The American Journal of Pathology, 169, 200–208.
Li, Y.L. & Jung, W.C. (2022) Reprogramming of sentinel lymph node microenvironment during tumor metastasis. Journal of Biomedical Science, 29, 84.
Lutz, M.B., Ali, S., Audiger, C., Autenrieth, S.E., Berod, L. & Bigley, V. (2022) Guidelines for mouse and human DC generation. European Journal of Immunology, 53, e2249816. Available from: https://doi.org/10.1002/eji.202249816
Marzaioli, V., Canavan, M., Floudas, A., Flynn, K., Mullan, R., Veale, D.J. et al. (2022) CD209/CD14+ dendritic cells characterization in rheumatoid and psoriatic arthritis patients: activation, synovial infiltration, and therapeutic targeting. Frontiers in Immunology, 12, 722349.
Pak, K.H., Park, K.C. & Cheong, J.H. (2019) VEGF‐C induced by TGF‐ß1 signaling in gastric cancer enhances tumor‐induced lymphangiogenesis. BMC Cancer, 19, 799.
Park, S.M., Angel, C.E., McIntosh, J., Mansell, C.M., Chen, C.J.J., Cebon, J. et al. (2014) Mapping the distinctive populations of lymphatic endothelial cells in different zones of human lymph nodes. PLoS One, 9, e94781.
Reis‐Sobreiro, M., da Mota, A.T., Jardim, C. & Serre, K. (2021) Bringing macrophages to the frontline against cancer: current immunotherapies targeting macrophages. Cells, 10, 2364. Available from: https://doi.org/10.3390/cells10092364
Riedel, A., Shorthouse, D., Haas, L., Hall, B.A. & Shields, J. (2016) Tumor induced stromal reprogramming drives lymph node transformation. Nature Immunology, 17, 1118–1127.
Takeuchi, H., Kitajima, M. & Kitagawa, Y. (2008) Sentinel lymph node as a target of molecular diagnosis of lymphatic micrometastasis and local immunoresponse to malignant cells. Cancer Science, 99, 441–450.
Tanaka, A. & Sakaguchi, S. (2017) Regulatory T cells in cancer immunotherapy. Cell Research, 27, 109–118.
Tay, C., Tanaka, A. & Sakaguchi, S. (2023) Tumor‐infiltrating regulatory T cells as targets of cancer immunotherapy. Cancer Cell, 41, 450–465.
van der Valk, P. & Meijer, C.J.L.M. (1997) Reactive lymph node. In: Histology for pathologists, 2nd edition. Philadelphia: Lippincott‐Raven, pp. 651–673.
van Pul, K.M., Vuylsteke, R.J.C.L.M., de Beijer, M.T.A., van de Ven, R., van den Tol, M.P., Stockmann, H.B.A.C. et al. (2020) Breast cancer‐induced immune suppression in the sentinel lymph node is effectively countered by CpG‐B in conjunction with inhibition of the JAK2/STAT3 pathway. J Immunother Cancer, 8, e000761.
Van Pul, K.M., Vuylsteke, R.J.C.L.M., De Ven, V., Te Velde, E.A., Th Rutgers, E.J., Van Den Tol, M.P. et al. (2019) Selectively hampered activation of lymph node‐ resident dendritic cells precedes profound T cell suppression and metastatic spread in the breast cancer sentinel lymph node. The Journal of Immunotherapy Cancer, 7, 133.
Virgilio, T., Bordini, J., Cascione, L., Sartori, G., Latino, I., Romero, D.M. et al. (2022) Subcapsular sinus macrophages promote melanoma metastasis to the sentinel lymph nodes via an IL1a‐STAT axis. Cancer Immunology Research, 10, 1525–1541.
Yamada, R., Ohnishi, K., Pan, C., Yano, H., Fujiwara, Y., Shiota, T. et al. (2023) Expression of macrophage/dendritic cell‐related molecules in lymph node sinus macrophages. Microbiology and Immunology, 67, 490–500. Available from: https://doi.org/10.1111/1348‐0421.13095