Splenectomy has opposite effects on the growth of primary compared with metastatic tumors in a murine colon cancer model.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 Feb 2024
24 Feb 2024
Historique:
received:
11
09
2023
accepted:
16
02
2024
medline:
25
2
2024
pubmed:
25
2
2024
entrez:
24
2
2024
Statut:
epublish
Résumé
The spleen is a key source of circulating and tumor-infiltrating immune cells. However, the effect of splenectomy on tumor growth remains unclear. At 3 weeks after splenectomy, we subcutaneously injected LuM1 cells into BALB/c mice and evaluated the growth of primary tumors and lung metastases at 4 weeks after tumor inoculation. In addition, we examined the phenotypes of immune cells in peripheral blood by using flow cytometry and in tumor tissue by using multiplex immunohistochemistry. The growth of primary tumors was reduced in splenectomized mice compared with the sham-operated group. Conversely, splenectomized mice had more lung metastases. Splenectomized mice had fewer CD11b
Identifiants
pubmed: 38402307
doi: 10.1038/s41598-024-54768-5
pii: 10.1038/s41598-024-54768-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4496Subventions
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Organisme : Japan Society for the Promotion of Science
ID : 21K08740
Informations de copyright
© 2024. The Author(s).
Références
Mebius, R. E. & Kraal, G. Structure and function of the spleen. Nat. Rev. Immunol. 5, 606–616. https://doi.org/10.1038/nri1669 (2005).
doi: 10.1038/nri1669
pubmed: 16056254
Linet, M. S. et al. Risk of cancer following splenectomy. Int. J. Cancer 66, 611–616. https://doi.org/10.1002/(SICI)1097-0215(19960529)66:5%3c611::AID-IJC5%3e3.0.CO;2-W (1996).
doi: 10.1002/(SICI)1097-0215(19960529)66:5<611::AID-IJC5>3.0.CO;2-W
pubmed: 8647621
Mellemkjoer, L., Olsen, J. H., Linet, M. S., Gridley, G. & McLaughlin, J. K. Cancer risk after splenectomy. Cancer 75, 577–583. https://doi.org/10.1002/1097-0142(19950115)75:2%3c577::aid-cncr2820750222%3e3.0.co;2-k (1995).
doi: 10.1002/1097-0142(19950115)75:2<577::aid-cncr2820750222>3.0.co;2-k
pubmed: 7812926
Griffith, J. P. et al. Preservation of the spleen improves survival after radical surgery for gastric cancer. Gut 36, 684–690. https://doi.org/10.1136/gut.36.5.684 (1995).
doi: 10.1136/gut.36.5.684
pubmed: 7797117
pmcid: 1382670
Wanebo, H. J., Kennedy, B. J., Winchester, D. P., Stewart, A. K. & Fremgen, A. M. Role of splenectomy in gastric cancer surgery: Adverse effect of elective splenectomy on longterm survival. J. Am. Coll. Surg. 185, 177–184 (1997).
doi: 10.1016/S1072-7515(01)00901-2
pubmed: 9249086
Davis, C. J., Ilstrup, D. M. & Pemberton, J. H. Influence of splenectomy on survival rate of patients with colorectal cancer. Am. J. Surg. 155, 173–179. https://doi.org/10.1016/s0002-9610(88)80276-9 (1988).
doi: 10.1016/s0002-9610(88)80276-9
pubmed: 3341531
Schwarz, R. E., Harrison, L. E., Conlon, K. C., Klimstra, D. S. & Brennan, M. F. The impact of splenectomy on outcomes after resection of pancreatic adenocarcinoma. J. Am. Coll. Surg. 188, 516–521. https://doi.org/10.1016/s1072-7515(99)00041-1 (1999).
doi: 10.1016/s1072-7515(99)00041-1
pubmed: 10235580
Michowitz, M., Donin, N., Sinai, J. & Leibovici, J. Comparison of splenectomy effects as an indication for host response to growth of primary and metastatic tumour cells in two murine tumour systems. Int. J. Exp. Pathol. 76, 13–19 (1995).
pubmed: 7734336
pmcid: 1997145
Levy, L. et al. Splenectomy inhibits non-small cell lung cancer growth by modulating anti-tumor adaptive and innate immune response. Oncoimmunology 4, e998469. https://doi.org/10.1080/2162402X.2014.998469 (2015).
doi: 10.1080/2162402X.2014.998469
pubmed: 26137413
pmcid: 4485806
Li, B. H. et al. The spleen contributes to the increase in PMN-MDSCs in orthotopic H22 hepatoma mice. Mol. Immunol. 125, 95–103. https://doi.org/10.1016/j.molimm.2020.07.002 (2020).
doi: 10.1016/j.molimm.2020.07.002
pubmed: 32659598
Imai, S. et al. Effects of splenectomy on pulmonary metastasis and growth of SC42 carcinoma transplanted into mouse liver. J. Surg. Oncol. 47, 178–187. https://doi.org/10.1002/jso.2930470309 (1991).
doi: 10.1002/jso.2930470309
pubmed: 2072702
Soda, K., Kawakami, M., Takagi, S., Kashii, A. & Miyata, M. Splenectomy before tumor inoculation prolongs the survival time of cachectic mice. Cancer Immunol. Immunother. 41, 203–209. https://doi.org/10.1007/bf01516994 (1995).
doi: 10.1007/bf01516994
pubmed: 7489562
Stöth, M. et al. Splenectomy reduces lung metastases and tumoral and metastatic niche inflammation. Int. J. Cancer 145, 2509–2520. https://doi.org/10.1002/ijc.32378 (2019).
doi: 10.1002/ijc.32378
pubmed: 31034094
Sevmis, M. et al. Splenectomy-induced leukocytosis promotes intratumoral accumulation of myeloid-derived suppressor cells, angiogenesis and metastasis. Immunol. Investig. 46, 663–676. https://doi.org/10.1080/08820139.2017.1360339 (2017).
doi: 10.1080/08820139.2017.1360339
Sato, N., Michaelides, M. C. & Wallack, M. K. Effect of splenectomy on the growth of murine colon tumors. J. Surg. Oncol. 22, 73–76. https://doi.org/10.1002/jso.2930220202 (1983).
doi: 10.1002/jso.2930220202
pubmed: 6823129
Hwang, H. K. et al. Splenectomy is associated with an aggressive tumor growth pattern and altered host immunity in an orthotopic syngeneic murine pancreatic cancer model. Oncotarget 8, 88827–88834. https://doi.org/10.18632/oncotarget.21331 (2017).
doi: 10.18632/oncotarget.21331
pubmed: 29179479
pmcid: 5687649
Kopel, S., Michowitz, M. & Leibovici, J. Effect of splenectomy on the efficiency of chemo-immunotherapy of melanoma-bearing mice. Int. J. Immunopharmacol. 7, 801–810. https://doi.org/10.1016/0192-0561(85)90042-6 (1985).
doi: 10.1016/0192-0561(85)90042-6
pubmed: 4077343
Shiratori, Y. et al. Effect of splenectomy on hepatic metastasis of colon carcinoma and natural killer activity in the liver. Dig. Dis. Sci. 40, 2398–2406. https://doi.org/10.1007/bf02063244 (1995).
doi: 10.1007/bf02063244
pubmed: 7587821
Higashijima, J. et al. Effect of splenectomy on antitumor immune system in mice. Anticancer Res. 29, 385–393 (2009).
pubmed: 19331177
Ron, Y., Gorelik, E., Feldman, M. & Segal, S. Effect of splenectomy on the progression of postoperative pulmonary metastases of the 3LL tumor. Eur. J. Cancer Clin. Oncol. 18, 391–397. https://doi.org/10.1016/0277-5379(82)90011-6 (1982).
doi: 10.1016/0277-5379(82)90011-6
pubmed: 6889517
Sonoda, K. et al. Decreased growth rate of lung metastatic lesions after splenectomy in mice. Eur. Surg. Res. 38, 469–475. https://doi.org/10.1159/000095415 (2006).
doi: 10.1159/000095415
pubmed: 16940732
Li, B. et al. Dynamics of the spleen and its significance in a murine H22 orthotopic hepatoma model. Exp. Biol. Med. (Maywood) 241, 863–872. https://doi.org/10.1177/1535370216638772 (2016).
doi: 10.1177/1535370216638772
pubmed: 26989085
Schwarz, R. E. & Hiserodt, J. C. Effects of splenectomy on the development of tumor-specific immunity. J. Surg. Res. 48, 448–453. https://doi.org/10.1016/0022-4804(90)90011-p (1990).
doi: 10.1016/0022-4804(90)90011-p
pubmed: 2352420
Prehn, R. T. The paradoxical effects of splenectomy on tumor growth. Theor. Biol. Med. Model. 3, 23. https://doi.org/10.1186/1742-4682-3-23 (2006).
doi: 10.1186/1742-4682-3-23
pubmed: 16800890
pmcid: 1538594
Bronte, V. & Pittet, M. J. The spleen in local and systemic regulation of immunity. Immunity 39, 806–818. https://doi.org/10.1016/j.immuni.2013.10.010 (2013).
doi: 10.1016/j.immuni.2013.10.010
pubmed: 24238338
pmcid: 3912742
Ng, L. G., Liu, Z., Kwok, I. & Ginhoux, F. Origin and heterogeneity of tissue myeloid cells: A focus on GMP-derived monocytes and neutrophils. Annu. Rev. Immunol. 41, 375–404. https://doi.org/10.1146/annurev-immunol-081022-113627 (2023).
doi: 10.1146/annurev-immunol-081022-113627
pubmed: 37126421
Gabrilovich, D. I. Myeloid-derived suppressor cells. Cancer Immunol. Res. 5, 3–8. https://doi.org/10.1158/2326-6066.CIR-16-0297 (2017).
doi: 10.1158/2326-6066.CIR-16-0297
pubmed: 28052991
pmcid: 5426480
Krishnamoorthy, M., Gerhardt, L. & Maleki Vareki, S. Immunosuppressive effects of myeloid-derived suppressor cells in cancer and immunotherapy. Cells https://doi.org/10.3390/cells10051170 (2021).
doi: 10.3390/cells10051170
pubmed: 34065010
pmcid: 8150533
Cortez-Retamozo, V. et al. Origins of tumor-associated macrophages and neutrophils. Proc. Natl. Acad. Sci. U. S. A. 109, 2491–2496. https://doi.org/10.1073/pnas.1113744109 (2012).
doi: 10.1073/pnas.1113744109
pubmed: 22308361
pmcid: 3289379
Gerstberger, S., Jiang, Q. & Ganesh, K. Metastasis. Cell 186, 1564–1579. https://doi.org/10.1016/j.cell.2023.03.003 (2023).
doi: 10.1016/j.cell.2023.03.003
pubmed: 37059065
pmcid: 10511214
Kubo, H., Mensurado, S., Goncalves-Sousa, N., Serre, K. & Silva-Santos, B. Primary tumors limit metastasis formation through induction of IL15-mediated cross-talk between patrolling monocytes and NK cells. Cancer Immunol. Res. 5, 812–820. https://doi.org/10.1158/2326-6066.CIR-17-0082 (2017).
doi: 10.1158/2326-6066.CIR-17-0082
pubmed: 28811289
Plebanek, M. P. et al. Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nat. Commun. 8, 1319. https://doi.org/10.1038/s41467-017-01433-3 (2017).
doi: 10.1038/s41467-017-01433-3
pubmed: 29105655
pmcid: 5673063
Sakata, K. et al. Establishment and characterization of high- and low-lung-metastatic cell lines derived from murine colon adenocarcinoma 26 tumor line. Jpn. J. Cancer Res. 87, 78–85. https://doi.org/10.1111/j.1349-7006.1996.tb00203.x (1996).
doi: 10.1111/j.1349-7006.1996.tb00203.x
pubmed: 8609053
pmcid: 5920974
Cassetta, L. & Pollard, J. W. Cancer immunosurveillance: Role of patrolling monocytes. Cell Res. 26, 3–4. https://doi.org/10.1038/cr.2015.144 (2016).
doi: 10.1038/cr.2015.144
pubmed: 26634605
Gamrekelashvili, J. et al. Regulation of monocyte cell fate by blood vessels mediated by Notch signalling. Nat. Commun. 7, 12597. https://doi.org/10.1038/ncomms12597 (2016).
doi: 10.1038/ncomms12597
pubmed: 27576369
pmcid: 5013671
Hanna, R. N. et al. Patrolling monocytes control tumor metastasis to the lung. Science 350, 985–990. https://doi.org/10.1126/science.aac9407 (2015).
doi: 10.1126/science.aac9407
pubmed: 26494174
pmcid: 4869713
Galon, J. et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960–1964. https://doi.org/10.1126/science.1129139 (2006).
doi: 10.1126/science.1129139
pubmed: 17008531
Mahmoud, S. M. et al. Tumor-infiltrating CD8
doi: 10.1200/jco.2010.30.5037
pubmed: 21483002
Fukunaga, A. et al. CD8
doi: 10.1097/00006676-200401000-00023
pubmed: 14707745
Yonesaka, K. et al. B7–H3 negatively modulates CTL-mediated cancer immunity. Clin. Cancer Res. 24, 2653–2664. https://doi.org/10.1158/1078-0432.Ccr-17-2852 (2018).
doi: 10.1158/1078-0432.Ccr-17-2852
pubmed: 29530936
Hao, H. et al. Icaritin promotes tumor T-cell infiltration and induces antitumor immunity in mice. Eur. J. Immunol. 49, 2235–2244. https://doi.org/10.1002/eji.201948225 (2019).
doi: 10.1002/eji.201948225
pubmed: 31465113
Moore, C. et al. Personalized ultrafractionated stereotactic adaptive radiotherapy (PULSAR) in preclinical models enhances single-agent immune checkpoint blockade. Int. J. Radiat. Oncol. Biol. Phys. 110, 1306–1316. https://doi.org/10.1016/j.ijrobp.2021.03.047 (2021).
doi: 10.1016/j.ijrobp.2021.03.047
pubmed: 33794306
pmcid: 8286324
Vanbuskirk, A., Oberyszyn, T. M. & Kusewitt, D. F. Depletion of CD8
pubmed: 16158931
Sierra-Filardi, E. et al. CCL2 shapes macrophage polarization by GM-CSF and M-CSF: Identification of CCL2/CCR2-dependent gene expression profile. J. Immunol. 192, 3858–3867. https://doi.org/10.4049/jimmunol.1302821 (2014).
doi: 10.4049/jimmunol.1302821
pubmed: 24639350
Cheng, J. N., Yuan, Y. X., Zhu, B. & Jia, Q. Myeloid-derived suppressor cells: A multifaceted accomplice in tumor progression. Front. Cell Dev. Biol. 9, 740827. https://doi.org/10.3389/fcell.2021.740827 (2021).
doi: 10.3389/fcell.2021.740827
pubmed: 35004667
pmcid: 8733653
Sanford, D. E. et al. Inflammatory monocyte mobilization decreases patient survival in pancreatic cancer: A role for targeting the CCL2/CCR2 axis. Clin. Cancer Res. 19, 3404–3415. https://doi.org/10.1158/1078-0432.Ccr-13-0525 (2013).
doi: 10.1158/1078-0432.Ccr-13-0525
pubmed: 23653148
pmcid: 3700620
Li, R., Wen, A. & Lin, J. Pro-inflammatory cytokines in the formation of the pre-metastatic niche. Cancers (Basel) https://doi.org/10.3390/cancers12123752 (2020).
doi: 10.3390/cancers12123752
pubmed: 33396603
pmcid: 8456613
Lakshmikanth, T. et al. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J. Clin. Investig. 119, 1251–1263. https://doi.org/10.1172/JCI36022 (2009).
doi: 10.1172/JCI36022
pubmed: 19349689
pmcid: 2673866
Halfteck, G. G. et al. Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J. Immunol. 182, 2221–2230. https://doi.org/10.4049/jimmunol.0801878 (2009).
doi: 10.4049/jimmunol.0801878
pubmed: 19201876
Glasner, A. et al. NKp46 receptor-mediated interferon-gamma production by natural killer cells increases fibronectin 1 to alter tumor architecture and control metastasis. Immunity 48, 396–398. https://doi.org/10.1016/j.immuni.2018.01.010 (2018).
doi: 10.1016/j.immuni.2018.01.010
pubmed: 29466761
pmcid: 5823842
Shimasaki, N., Jain, A. & Campana, D. NK cells for cancer immunotherapy. Nat. Rev. Drug Discov. 19, 200–218. https://doi.org/10.1038/s41573-019-0052-1 (2020).
doi: 10.1038/s41573-019-0052-1
pubmed: 31907401
Zhu, M. et al. Evasion of innate immunity contributes to small cell lung cancer progression and metastasis. Cancer Res. 81, 1813–1826. https://doi.org/10.1158/0008-5472.CAN-20-2808 (2021).
doi: 10.1158/0008-5472.CAN-20-2808
pubmed: 33495232
pmcid: 8137539
Chan, I. S. & Ewald, A. J. The changing role of natural killer cells in cancer metastasis. J. Clin. Investig. https://doi.org/10.1172/JCI143762 (2022).
doi: 10.1172/JCI143762
pubmed: 36201246
pmcid: 9663158
Lo, H. C. et al. Resistance to natural killer cell immunosurveillance confers a selective advantage to polyclonal metastasis. Nat. Cancer 1, 709–722. https://doi.org/10.1038/s43018-020-0068-9 (2020).
doi: 10.1038/s43018-020-0068-9
pubmed: 35122036
Vyas, M. et al. Natural killer cells suppress cancer metastasis by eliminating circulating cancer cells. Front. Immunol. 13, 1098445. https://doi.org/10.3389/fimmu.2022.1098445 (2022).
doi: 10.3389/fimmu.2022.1098445
pubmed: 36733396
Wang, B. et al. A novel spleen-resident immature NK cell subset and its maturation in a T-bet-dependent manner. J. Autoimmun. 105, 102307. https://doi.org/10.1016/j.jaut.2019.102307 (2019).
doi: 10.1016/j.jaut.2019.102307
pubmed: 31351783
Yamamoto, M. et al. Established gastric cancer cell lines transplantable into C57BL/6 mice show fibroblast growth factor receptor 4 promotion of tumor growth. Cancer Sci. 109, 1480–1492. https://doi.org/10.1111/cas.13569 (2018).
doi: 10.1111/cas.13569
pubmed: 29532565
pmcid: 5980194
Kumagai, Y. et al. Effect of systemic or intraperitoneal administration of anti-PD-1 antibody for peritoneal metastases from gastric cancer. In Vivo 36, 1126–1135. https://doi.org/10.21873/invivo.12811 (2022).
doi: 10.21873/invivo.12811
pubmed: 35478147
pmcid: 9087086
Wei, Y. et al. Abnormalities of the composition of the gut microbiota and short-chain fatty acids in mice after splenectomy. Brain Behav. Immun. Health 11, 100198. https://doi.org/10.1016/j.bbih.2021.100198 (2021).
doi: 10.1016/j.bbih.2021.100198
pubmed: 34589731
pmcid: 8474575
Tsujikawa, T. et al. Quantitative multiplex immunohistochemistry reveals myeloid-inflamed tumor-immune complexity associated with poor prognosis. Cell Rep. 19, 203–217. https://doi.org/10.1016/j.celrep.2017.03.037 (2017).
doi: 10.1016/j.celrep.2017.03.037
pubmed: 28380359
pmcid: 5564306