Skip to main content

Advertisement

SpringerLink
Log in

Chronic Inflammation Contributes to Tumor Growth: Possible Role of l-Selectin-Expressing Myeloid-Derived Suppressor Cells (MDSCs)

  • ORIGINAL ARTICLE
  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

Recent data have demonstrated that chronic inflammation is a crucial component of tumor initiation and progression. We previously reported that immature myeloid-derived suppressor cells (MDSCs) with immunosuppressive activity toward effector T cells were expanded in experimental chronic inflammation. We hypothesized that elevated levels of MDSCs, induced by chronic inflammation, may contribute to the progression of tumor growth. Using the Ehrlich carcinoma animal model, we found increased tumor growth in mice with chronic adjuvant arthritis, which was accompanied by a persistent increase in the proportion of splenic monocytic and granulocytic MDSCs expressing CD62L (l-selectin), when compared to tumor mice without adjuvant arthritis. Depletion of inflammation-induced MDSCs resulted in decreased tumor growth. In vitro studies demonstrated that increased expression of CD62L by MDSCs was mediated by TNFα, elevated concentrations of which were found in tumor mice subjected to chronic inflammation. Moreover, the addition of exogenous TNFα markedly enhanced the suppressive activity of bone marrow-derived MDSCs, as revealed by the ability to impair the proliferation of CD8+ T cells in vitro. This study provides evidence that chronic inflammation may promote tumor growth via induction of CD62L expression by MDSCs that can facilitate their migration to tumor and lymph nodes and modulation of their suppressor activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AA:

Arthritic animals

Ab:

Antibody

APC:

Allophycocyanin

Arg-1:

Arginase-1

ATA:

Arthritic animals with tumor

BM:

Bone marrow

CA:

Control animals

CFA:

Complete Freund’s adjuvant

CFSE:

5(6)-Carboxyfluorescein diacetate N-succinimidyl ester

ConA:

Concanavalin A

CXCR4:

C-X-C chemokine receptor type 4

DCFDA:

2′-7′-dichlorofluorescein diacetate

EDTA:

Ethylenediaminetetraacetic acid

ELISA:

Enzyme-linked immunosorbent assay

FBS:

Fetal bovine serum

FITC:

Fluorescein isothiocyanate

GHVD:

Graft-versus-host disease

GM-CSF:

Granulocyte-macrophage colony-stimulating factor

HIV:

Human immunodeficiency virus

IFNγ:

Interferon gamma

IL:

Interleukin

iNOS:

Inducible nitric oxide synthase

LBS:

Lysing buffer solution

MCP-1:

Monocyte chemoattractant protein-1

MDSC:

Myeloid-derived suppressor cells

MIP-1α:

Macrophage inflammatory protein 1 alpha

NF-κB:

Nuclear factor kappa B

NO:

Nitric oxide

PE:

Phycoerythrin

PerCP:

Peridinin chlorophyll protein complex

PGE2:

Prostaglandin E2

RAGE:

Receptor for advanced glycation end products

ROS:

Reactive oxygen species

SDF-1α:

Stromal cell-derived factor one alpha

TA:

Tumor animals

TGFβ:

Transforming growth factor beta

TLR:

Toll-like receptors

TNFα:

Tumor necrosis factor alpha

VEGF:

Vascular endothelial growth factor

References

  1. Multhoff, G., M. Molls, and J. Radons. 2012. Chronic inflammation in cancer development. Frontiers in Immunology 2: 98. https://doi.org/10.3389/fimmu.2011.00098.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Wang, Dingzhi, and Raymond N. DuBois. 2015. Immunosuppression associated with chronic inflammation in the tumor microenvironment. Carcinogenesis 36: 1085–1093. https://doi.org/10.1093/carcin/bgv123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bronte, Vincenzo, Sven Brandau, Shu Hsia Chen, Mario P. Colombo, Alan B. Frey, Tim F. Greten, Susanna Mandruzzato, Peter J. Murray, Augusto Ochoa, Suzanne Ostrand-Rosenberg, Paulo C. Rodriguez, Antonio Sica, Viktor Umansky, Robert H. Vonderheide, and Dmitry I. Gabrilovich. 2016. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nature Communications 7: 12150. https://doi.org/10.1038/ncomms12150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Xia, Sheng, Haibo Sha, Liu Yang, Yewei Ji, Suzanne Ostrand-Rosenberg, and Ling Qi. 2011. Gr-1+ CD11b+ myeloid-derived suppressor cells suppress inflammation and promote insulin sensitivity in obesity. Journal of Biological Chemistry 286: 23591–23599. https://doi.org/10.1074/jbc.M111.237123.

    Article  CAS  PubMed  Google Scholar 

  5. Höchst, Bastian, Julita Mikulec, Tania Baccega, Christina Metzger, Meike Welz, Julia Peusquens, Frank Tacke, Percy Knolle, Christian Kurts, Linda Diehl, and Isis Ludwig-Portugall. 2015. Differential induction of Ly6G and Ly6C positive myeloid derived suppressor cells in chronic kidney and liver inflammation and fibrosis. PLoS One 10: e0119662. https://doi.org/10.1371/journal.pone.0119662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Singh, Udai P., Narendra P. Singh, Balwan Singh, Lorne J. Hofseth, Dennis D. Taub, Robert L. Price, Mitzi Nagarkatti, and Prakash S. Nagarkatti. 2012. Role of resveratrol-induced CD11b(+) Gr-1(+) myeloid derived suppressor cells (MDSCs) in the reduction of CXCR3(+) T cells and amelioration of chronic colitis in IL-10(-/-) mice. Brain, Behavior, and Immunity 26: 72–82. https://doi.org/10.1016/j.bbi.2011.07.236.

    Article  CAS  PubMed  Google Scholar 

  7. Obregón-Henao, Andrés, Marcela Henao-Tamayo, Ian M. Orme, and Diane J. Ordway. 2013. Gr1intCD11b+ myeloid-derived suppressor cells in mycobacterium tuberculosis infection. PLoS One 8: e80669. https://doi.org/10.1371/journal.pone.0080669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Vollbrecht, Thomas, Renate Stirner, Amanda Tufman, Julia Roider, Rudolf M. Huber, Johannes R. Bogner, Andreas Lechner, Carole Bourquin, and Rika Draenert. 2012. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 26. https://doi.org/10.1097/QAD.0b013e328354b43f.

  9. Dorhoi, Anca, and Nelita Du Plessis. 2017. Monocytic myeloid-derived suppressor cells in chronic infections. Front Immunol 8:1895. doi:https://doi.org/10.3389/fimmu.2017.01895.

  10. Verschoor, C.P., J. Johnstone, J. Millar, M.G. Dorrington, M. Habibagahi, A. Lelic, M. Loeb, J.L. Bramson, and D.M.E. Bowdish. 2013. Blood CD33(+)HLA-DR(-) myeloid-derived suppressor cells are increased with age and a history of cancer. Journal of Leukocyte Biology 93: 633–637. https://doi.org/10.1189/jlb.0912461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Flores, Rafael R., Cheryl L. Clauson, Joonseok Cho, Byeong Chel Lee, Sara J. McGowan, Darren J. Baker, Laura J. Niedernhofer, and Paul D. Robbins. 2017. Expansion of myeloid-derived suppressor cells with aging in the bone marrow of mice through a NF-κB-dependent mechanism. Aging Cell 16: 480–487. https://doi.org/10.1111/acel.12571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Perfilyeva, Yuliya V., Nurshat Abdolla, Yekaterina O. Ostapchuk, Raikhan Tleulieva, Vladimir C. Krasnoshtanov, and Nikolai N. Belyaev. 2017. Expansion of CD11b(+)Ly6G(high) and CD11b(+)CD49d(+) myeloid cells with suppressive potential in mice with chronic inflammation and light-at-night-induced circadian disruption. Inflammation Research 66 (8): 711–724. https://doi.org/10.1007/s00011-017-1052-4.

    Article  CAS  PubMed  Google Scholar 

  13. Zhang, Hui, Shuang Wang, Yuefang Huang, Hongyue Wang, Jijun Zhao, Felicia Gaskin, Niansheng Yang, and Shu Man Fu. 2015. Myeloid-derived suppressor cells are proinflammatory and regulate collagen-induced arthritis through manipulating Th17 cell differentiation. Clinical Immunology 157: 175–186. https://doi.org/10.1016/j.clim.2015.02.001.

    Article  CAS  PubMed  Google Scholar 

  14. Guo, Chunqing, Hu Fanlei, Huanfa Yi, Zhitao Feng, Changzheng Li, Lianjie Shi, Yingni Li, et al. 2014. Myeloid-derived suppressor cells have a proinflammatory role in the pathogenesis of autoimmune arthritis. Annals of the Rheumatic Diseases 75 (1): 278–285. https://doi.org/10.1136/annrheumdis-2014-205508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhan, Xiaoxia, Yimin Fang, Shengfeng Hu, Yongjian Wu, Kun Yang, Chunxin Liao, Yuanqing Zhang, Xi Huang, and Minhao Wu. 2015. IFN-γ differentially regulates subsets of Gr-1+CD11b+ myeloid cells in chronic inflammation. Molecular Immunology 66: 451–462. https://doi.org/10.1016/j.molimm.2015.05.011.

    Article  CAS  PubMed  Google Scholar 

  16. Poh, Tze Wei, Cathy S. Madsen, Jessica E. Gorman, Ronald J. Marler, Jonathan A. Leighton, Peter A. Cohen, and Sandra J. Gendler. 2013. Downregulation of hematopoietic MUC1 during experimental colitis increases tumor-promoting myeloid-derived suppressor cells. Clinical Cancer Research 19: 5039–5052. https://doi.org/10.1158/1078-0432.CCR-13-0278.

    Article  CAS  PubMed  Google Scholar 

  17. Katoh, Hiroshi, Dingzhi Wang, Takiko Daikoku, Haiyan Sun, Sudhansu K. Dey, and Raymond N. DuBois. 2013. CXCR2-expressing myeloid-derived suppressor cells are essential to promote colitis-associated tumorigenesis. Cancer Cell 24: 631–644. https://doi.org/10.1016/j.ccr.2013.10.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wang, Zibing, Jing Jiang, Zhiguang Li, Jinhua Zhang, Hui Wang, and Zhihai Qin. 2010. A myeloid cell population induced by Freund adjuvant suppresses T-cell-mediated antitumor immunity. Journal of Immunotherapy 33: 167–177. https://doi.org/10.1097/CJI.0b013e3181bed2ba.

    Article  CAS  PubMed  Google Scholar 

  19. Ostrand-Rosenberg, Suzanne, and Pratima Sinha. 2009. Myeloid-derived suppressor cells: linking inflammation and cancer. Journal of Immunology 182: 4499–4506. https://doi.org/10.4049/jimmunol.0802740.

    Article  CAS  Google Scholar 

  20. Zhao, Xueqiang, Lijie Rong, Xiaopu Zhao, Xiao Li, Xiaoman Liu, Jingjing Deng, Wu Hao, et al. 2012. TNF signaling drives myeloid-derived suppressor cell accumulation. Journal of Clinical Investigation 122: 4094–4104. https://doi.org/10.1172/JCI64115.

    Article  CAS  PubMed  Google Scholar 

  21. Sade-Feldman, Moshe, Julia Kanterman, Eliran Ish-Shalom, Mazal Elnekave, Elad Horwitz, and Michal Baniyash. 2013. Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 38: 541–554. https://doi.org/10.1016/j.immuni.2013.02.007.

    Article  CAS  PubMed  Google Scholar 

  22. Marigo, Ilaria, Erika Bosio, Samantha Solito, Circe Mesa, Audry Fernandez, Luigi Dolcetti, Stefano Ugel, Nada Sonda, Silvio Bicciato, Erika Falisi, Fiorella Calabrese, Giuseppe Basso, Paola Zanovello, Emanuele Cozzi, Susanna Mandruzzato, and Vincenzo Bronte. 2010. Tumor-induced tolerance and immune suppression depend on the C/EBPβ transcription factor. Immunity 32: 790–802. https://doi.org/10.1016/j.immuni.2010.05.010.

    Article  CAS  PubMed  Google Scholar 

  23. Le, Hanh K., Laura Graham, Esther Cha, Johanna K. Morales, Masoud H. Manjili, and Harry D. Bear. 2009. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Intl Immunopharmacol 9 (7–8): 900–909. https://doi.org/10.1016/j.intimp.2009.03.015.

    Article  CAS  Google Scholar 

  24. Kumar, Vinit, Sima Patel, Evgenii Tcyganov, and Dmitry I. Gabrilovich. 2016. The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends in Immunology 37 (3): 208–220. https://doi.org/10.1016/j.it.2016.01.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Xiang, Xiaoyu, Yuelong Liu, Xiaoyin Zhuang, Shuangqin Zhang, Sue Michalek, Douglas D. Taylor, William Grizzle, and Huang Ge Zhang. 2010. TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. American Journal of Pathology 177: 1606–1610. https://doi.org/10.2353/ajpath.2010.100245.

    Article  CAS  PubMed  Google Scholar 

  26. Ray, Anuradha, Krishnendu Chakraborty, and Prabir Ray. 2013. Immunosuppressive MDSCs induced by TLR signaling during infection and role in resolution of inflammation. Frontiers in Cellular and Infection Microbiology 3. https://doi.org/10.3389/fcimb.2013.00052.

  27. Yu, Xiaowen, Jie Zeng, and Jianping Xie. 2014. Navigating through the maze of TLR2 mediated signaling network for better mycobacterium infection control. Biochimie 102: 1–8. https://doi.org/10.1016/j.biochi.2014.02.012.

    Article  CAS  PubMed  Google Scholar 

  28. Gabay, Cem. 2006. Interleukin-6 and chronic inflammation. Arthritis Research and Therapy 8: S3. https://doi.org/10.1186/ar1917.

    Article  CAS  PubMed  Google Scholar 

  29. Lukens, John R., Jordan M. Gross, and Thirumala Devi Kanneganti. 2012. IL-1 family cytokines trigger sterile inflammatory disease. Frontiers in Immunology 3: 315. https://doi.org/10.3389/fimmu.2012.00315.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Popa, C., M. G. Netea, P. L. C. M. van Riel, J. W. M. van der Meer, and A. F. H. Stalenhoef. 2007. The role of TNF-in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. The Journal of Lipid Research 48: 751–762. doi:https://doi.org/10.1194/jlr.R600021-JLR200.

  31. Kim, Ryungsa, Manabu Emi, Kazuaki Tanabe, and Koji Arihiro. 2006. Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Research 66 (11): 5527–5536. https://doi.org/10.1158/0008-5472.CAN-05-4128.

    Article  CAS  PubMed  Google Scholar 

  32. Gargett, Tessa, Susan N. Christo, Timothy R. Hercus, Nazim Abbas, Nimit Singhal, Angel F. Lopez, and Michael P. Brown. 2016. GM-CSF signalling blockade and chemotherapeutic agents act in concert to inhibit the function of myeloid-derived suppressor cells in vitro. Clinical & Translational Immunology 5: e119. https://doi.org/10.1038/cti.2016.80.

    Article  CAS  Google Scholar 

  33. Baniyash, Michal. 2006. Chronic inflammation, immunosuppression and cancer: New insights and outlook. Seminars in Cancer Biology 16 (1): 80–88. https://doi.org/10.1016/j.semcancer.2005.12.002.

    Article  CAS  PubMed  Google Scholar 

  34. Springer, Timothy A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76 (2): 301–314. https://doi.org/10.1016/0092-8674(94)90337-9.

    Article  CAS  Google Scholar 

  35. Garrood, T., L. Lee, and Costantino Pitzalis. 2006. Molecular mechanisms of cell recruitment to inflammatory sites: General and tissue-specific pathways. Rheumatology 45 (3): 250–260. https://doi.org/10.1093/rheumatology/kei207.

    Article  CAS  PubMed  Google Scholar 

  36. Highfill, Steven L., Paulo C. Rodriguez, Qing Zhou, Christine A. Goetz, Brent H. Koehn, Rachelle Veenstra, Patricia A. Taylor, A. Panoskaltsis-Mortari, J.S. Serody, D.H. Munn, J. Tolar, A.C. Ochoa, and B.R. Blazar. 2010. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 116: 5738–5747. https://doi.org/10.1182/blood-2010-06-287839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Liechtenstein, Therese, Noemi Perez-Janices, Maria Gato, Fabio Caliendo, Grazyna Kochan, Idoia Blanco-Luquin, Frederick Arce, et al. 2014. A highly efficient tumor-infiltrating MDSC differentiation system for discovery of anti-neoplastic targets, which circumvents the need for tumor establishment in mice. Oncotarget 5: 7843–7857. https://doi.org/10.18632/oncotarget.2279.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Liu, Xing, Ming Yang, Ligang Chen, Lilei Peng, Qiang Ye, Shuzhan Zheng, and Zhongcai Fan. 2012. TNF-α and G-CSF induce CD62L and CD106 expressions on rat bone marrow-derived MSCs. Asian Biomedicine 6 (3): 453–458. https://doi.org/10.5372/1905-7415.0603.076.

    Article  CAS  Google Scholar 

  39. Yang, Li, Jianhua Huang, Xiubao Ren, Agnieszka E. Gorska, Anna Chytil, Mary Aakre, David P. Carbone, Lynn M. Matrisian, Ann Richmond, P. Charles Lin, and Harold L. Moses. 2008. Abrogation of TGFβ signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13: 23–35. https://doi.org/10.1016/j.ccr.2007.12.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Obermajer, Nataša, Ravikumar Muthuswamy, Kunle Odunsi, Robert P. Edwards, and Pawel Kalinski. 2011. PGE 2-induced CXCL 12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Research 71: 7463–7470. https://doi.org/10.1158/0008-5472.CAN-11-2449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hiratsuka, Sachie, Dan G. Duda, Yuhui Huang, Shom Goel, Tatsuki Sugiyama, Takashi Nagasawa, Dai Fukumura, and Rakesh K. Jain. 2011. C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (Gr-1)-positive cells. Proceedings of the National Academy of Sciences of the United States of America 108: 302–307. https://doi.org/10.1073/pnas.1016917108.

    Article  PubMed  Google Scholar 

  42. Haribabu, Bodduluri, Ricardo M. Richardson, Ian Fisher, Silvano Sozzani, Stephen C. Peiper, Richard Horuk, Hydar Ali, and Ralph Snyderman. 1997. Regulation of human chemokine receptors CXCR4: Role of phosphorylation in desensitization and internalization. Journal of Biological Chemistry 272: 28726–28731. https://doi.org/10.1074/jbc.272.45.28726.

    Article  CAS  PubMed  Google Scholar 

  43. Maruyama, Akira, Hiroaki Shime, Yohei Takeda, Masahiro Azuma, Misako Matsumoto, and Tsukasa Seya. 2015. Pam2 lipopeptides systemically increase myeloid-derived suppressor cells through TLR2 signaling. Biochemical and Biophysical Research Communications 457: 445–450. https://doi.org/10.1016/j.bbrc.2015.01.011.

    Article  CAS  PubMed  Google Scholar 

  44. Chalmin, Fanny, Sylvain Ladoire, Grégoire Mignot, Julie Vincent, Mélanie Bruchard, Jean Paul Remy-Martin, Wilfrid Boireau, Alain Rouleau, Benoit Simon, David Lanneau, Aurélie de Thonel, Gabriele Multhoff, Arlette Hamman, François Martin, Bruno Chauffert, Eric Solary, Laurence Zitvogel, Carmen Garrido, Bernhard Ryffel, Christophe Borg, Lionel Apetoh, Cédric Rébé, and François Ghiringhelli. 2010. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. Journal of Clinical Investigation 120: 457–471. https://doi.org/10.1172/JCI40483.

    Article  CAS  PubMed  Google Scholar 

  45. Shime, Hiroaki, Akira Maruyama, Sumito Yoshida, Yohei Takeda, Misako Matsumoto, and Tsukasa Seya. 2017. Toll-like receptor 2 ligand and interferon-γ suppress anti-tumor T cell responses by enhancing the immunosuppressive activity of monocytic myeloid-derived suppressor cells. Oncoimmunology 7 (1): e1373231. https://doi.org/10.1080/2162402X.2017.1373231.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bosisio, Daniela, Nadia Polentarutti, Marina Sironi, Sergio Bernasconi, Kensuke Miyake, Ginette R. Webb, Michael U. Martin, Alberto Mantovani, and Marta Muzio. 2002. Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-y: A molecular basis for priming and synergism with bacterial lipopolysaccharide. Blood 99 (9): 3427–3431.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Theodore Micceri, Ph.D for critical reading of the manuscript.

Funding

This study was supported by the Grant No. AP05131710 “Pharmacological approaches to target myeloid-derived suppressor cells (MDSCs) for suppression of chronic inflammation as a stimulant of tumor growth in experimental models” of the Committee of Science of Ministry of Education and Science of the Republic of Kazakhstan.

Author information

Authors and Affiliations

  1. Laboratory of Molecular Immunology and Immunobiotechnology, M.A. Aitkhozhin’s Institute of Molecular Biology and Biochemistry, Almaty, Kazakhstan

    Yuliya V. Perfilyeva, Nurshat Abdolla, Yekaterina O. Ostapchuk & Raikhan Tleulieva

  2. Al-Farabi Kazakh National University, Almaty, Kazakhstan

    Nurshat Abdolla

  3. Kazakh Research Institute of Oncology & Radiology, Almaty, Kazakhstan

    Vladimir C. Krasnoshtanov

  4. Institute of General Genetics and Cytology, Laboratory of Molecular Genetics, Almaty, Kazakhstan

    Anastassiya V. Perfilyeva

  5. Saint-Petersburg Pasteur Institute, Saint-Petersburg, Russia

    Nikolai N. Belyaev

Authors
  1. Yuliya V. Perfilyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nurshat Abdolla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yekaterina O. Ostapchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Raikhan Tleulieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vladimir C. Krasnoshtanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anastassiya V. Perfilyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nikolai N. Belyaev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuliya V. Perfilyeva.

Ethics declarations

All experiments were carried out in compliance with the Guide for Care and Use of Laboratory Animals and approved by the Ethical Committee of M.A. Aitkhozhin’s Institute of Molecular Biology and Biochemistry, Almaty, Kazakhstan.

Conflict of Interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Perfilyeva, Y.V., Abdolla, N., Ostapchuk, Y.O. et al. Chronic Inflammation Contributes to Tumor Growth: Possible Role of l-Selectin-Expressing Myeloid-Derived Suppressor Cells (MDSCs). Inflammation 42, 276–289 (2019). https://doi.org/10.1007/s10753-018-0892-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-018-0892-6

KEY WORDS

Search

Navigation