Granulocyte colony-stimulating factor induces the migration of non-resident cells to intracerebral hemorrhage

Authors

DOI:

https://doi.org/10.14739/2310-1210.2023.6.287456

Keywords:

intracerebral hemorrhage, granulocyte colony-stimulating growth factor, CD44, CD68, CD146

Abstract

The aim of the study is to determine the effect of granulocyte colony-stimulating factor (rHuG-CSF) on the migration of non-resident cells into the region of intracerebral hemorrhage (ICH), which can potentially be considered as mesenchymal stem cells.

Materials and methods. In the experiment, unilateral ICH was simulated in rats by injection of autologous blood into the right hemisphere. Immunohistochemical method was used to study perihematomal area on day 1, 3, 10, 30, and 60 after ICH modeling. The appearance of cells expressing CD44, CD68, and CD146 markers was evaluated on a 3-point scale after penetrating trauma (PT) of the brain, ICH, and ICH with the growth factor injection (ICH/rHuG-CSF).

Results. In contrast to PT, ICH intensified the infiltration of CD44+ cells in the perihematomal area of the brain and caused the appearance of CD68+ and CD146+ cells in hemorrhage. The specific density of CD44+ cells was decreased on day 60 after ICH, and the effect of rHuG-CSF consisted in reducing the density of CD44+ cells on days 30 and 60. The appearance of CD68+ and CD146+ cells in the perihematomal area was seen after 10 days and further their detection was rare, while after the rHuG-CSF injection, the infiltration by cells with a similar immunophenotype was detected on day 3 ICH with a tendency to accumulate.

Conclusions. Infiltration by cells expressing CD44, CD68, and CD146 into the perihematomal area of the rat brain was heterogeneous as to the time after brain injury. The appearance of cells with specified immunophenotype could be associated with hematoma elimination, angiogenesis processes, and other mechanisms of the perihematomal brain region remodeling, in which mesenchymal stem cells were involved. rHuG-CSF modulated the migration of CD68+ and CD146+ cells, which consisted in their earlier and more intense migration to the damaged area of the brain after ICH.

Author Biographies

A. V. Kuraieva, Bogomolets National Medical University, Kyiv, Ukraine

PhD student of the Department of Histology and Embryology

S. I. Savosko, Bogomolets National Medical University, Kyiv, Ukraine

PhD, Associate Professor of the Department of Histology and Embryology

O. M. Grabovoy, Bogomolets National Medical University, Kyiv, Ukraine

MD, PhD, DSc, Professor of the Department of Histology and Embryology

O. M. Makarenko, Private Joint-Stock Company “Higher education institution “Interregional Academy of Personnel Management”, Kyiv, Ukraine

MD, PhD, DSc, Professor of the Department of General Medical Disciplines

References

Harris, D. T. (2014). Stem Cell Banking for Regenerative and Personalized Medicine. Biomedicines, 2(1), 50-79. https://doi.org/10.3390/biomedicines2010050

Ercelen, N., Karasu, N., Kahyaoglu, B., Cerezci, O., Akduman, R.C., Ercelen, D., Erturk, G., Gulay, G., Alpaydin, N., Boyraz, G., Monteleone, B., Kural, Z., Silek, H., Temur, S., & Bingol, C. A. (2023). Clinical experience: Outcomes of mesenchymal stem cell transplantation in five stroke patients. Frontiers in Medicine, 10, 1051831. https://doi.org/10.3389/fmed.2023.1051831

Tajiri, N., Kaneko, Y., Shinozuka, K., Ishikawa, H., Yankee, E., McGrogan, M., Case, C., & Borlongan, C. V. (2023). Stem cell recruitment of newly formed host cells via a successful seduction? Filling the gap between neurogenic niche and injured brain site. PLoS One, 8(9), e74857. https://doi.org/10.1371/journal.pone.0074857

Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nature Medicine, 8(9), 963-970. https://doi.org/10.1038/nm747

Rolfe, A., & Sun, D. (2015). Stem cell therapy in brain trauma: Implications for repair and regeneration of injured brain in experimental TBI models. In Brain Neurotrauma: Molecular, Neuropsychological, and Rehabilitation Aspects (pp. 587–596). CRC Press. https://doi.org/10.1201/b18126

Bernitz, J. M., Daniel, M. G., Fstkchyan, Y. S., & Moore, K. (2017). Granulocyte colony-stimulating factor mobilizes dormant hematopoietic stem cells without proliferation in mice. Blood, 129(14), 1901-1912. https://doi.org/10.1182/blood-2016-11-752923

Chen, Y., & Rudolph, K. L. (2021). Granulocyte colony-stimulating factor acts on lymphoid-biased, short-term hematopoietic stem cells. Haematologica, 106(6), 1516-1518. https://doi.org/10.3324/haematol.2020.271205

Kaur, S., Sehgal, A., Wu, A. C., Millard, S. M., Batoon, L., Sandrock, C. J., Ferrari-Cestari, M., Levesque, J. P., Hume, D. A., Raggatt, L. J., & Pettit, A. R. (2021). Stable colony-stimulating factor 1 fusion protein treatment increases hematopoietic stem cell pool and enhances their mobilisation in mice. Journal of Hematology & Oncology, 14(1), 3. https://doi.org/10.1186/s13045-020-00997-w

Lee, S., Im, S. A., Yoo, E. S., Nam, E. M., Lee, M. A., Ahn, J. Y., Huh, J. W., Kim, D. Y., Lee, S. N., Kim, M. J., Lee, S. J., Chung, W. S., & Seong, C. M. (2000). Mobilization kinetics of CD34(+) cells in association with modulation of CD44 and CD31 expression during continuous intravenous administration of G-CSF in normal donors. Stem Cells, 18(4), 281-286. https://doi.org/10.1634/stemcells.18-4-281

Shaida, Е. V., Klymniyk, G. I., Pavlyk, S. V., Khranovskaya, N. N., & Skachkova, O. V. (2013). Primenenie pegfilgrastima dlya mobilizatsii stvolovykh kletok perifericheskoi krovi u detei s solidnymi zlokachestvennymi novoobrazovaniyami [Peripheral blood stem cell mobilization with pegfilgrastim in children with solid malignancies]. Klinicheskaya onkologiya, (3), 88-90. [in Russian].

Szmigielska-Kaplon, A., Szemraj, J., Hamara, K., Robak, M., Wolska, A., Pluta, A., Czemerska, M., Krawczynska, A., Jamroziak, K., Szmigielska, K., Robak, T., & Wierzbowska, A. (2014). Polymorphism of CD44 influences the efficacy of CD34(+) cells mobilization in patients with hematological malignancies. Biology of Blood and Marrow Transplantation, 20(7), 986-991. https://doi.org/10.1016/j.bbmt.2014.03.019

Schabitz, W. R., Kollmar, R., Schwaninger, M., Juettler, E., Bardutzky, J., Scholzke, M. N., Sommer, C. & Schwab, S. (2003). Neuroprotective effect of granulocyte colony stimulating factor after focal cerebral ischemia. Stroke, 34(3), 745-751. https://doi.org/10.1161/01.STR.0000057814.70180.17

Qiu, X., Ping, S., Kyle, M., Chin, L., & Zhao, L.-R. (2023). Stem Cell Factor and Granulocyte Colony-Stimulating Factor Promote Remyelination in the Chronic Phase of Severe Traumatic Brain Injury. Cells, 12(5), 705. https://doi.org/10.3390/cells12050705

Modi, J., Menzie-Suderam, J., Xu, H., Trujillo, P., Medley, K., Marshall, M. L., Tao, R., Prentice, H., & Wu, J. Y. (2020). Mode of action of granulocyte-colony stimulating factor (G-CSF) as a novel therapy for stroke in a mouse model. Journal of Biomedical Science, 27(1), 19. https://doi.org/10.1186/s12929-019-0597-7

Kleinschnitz, C., Schroeter, M., Jander, S., & Stoll, G. (2004). Induction of granulocyte colony-stimulating factor mRNA by focal cerebral ischemia and cortical spreading depression. Brain research. Molecular brain research, 131(1-2), 73-78. https://doi.org/10.1016/j.molbrainres.2004.08.011

Schneider, A., Kruger C., Steigleder T., Weber, D., Pitzer, C., Laage, R., Aronowski, J., Maurer, M. H., Gassler, N., Mier, W., Hasselblatt, M., Kollmar, R., Schwab, S., Sommer, C., Bach, A., Kuhn, H. G. & Schabitz, A. W. (2005). The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. Journal of Clinical Investigation, 115(8), 2083-2098. https://doi.org/10.1172/JCI23559

Sawada, R., Nakano-Doi, A., Matsuyama, T., Nakagomi, N., & Nakagomi, T. (2020). CD44 expression in stem cells and niche microglia/macrophages following ischemic stroke. Stem Cell investigation, 7, 4. https://doi.org/10.21037/sci.2020.02.02

Zhang, G., Zhang, H., Liu, Y., He, Y., Wang, W., Du, Y., Yang, C., & Gao, F. (2014). CD44 clustering is involved in monocyte differentiation. Acta biochimica et biophysica Sinica (Shanghai), 46(7), 540-547. https://doi.org/10.1093/abbs/gmu042

Katayama, Y., Hidalgo, A., Chang, J., Peired, A., & Frenette, P. S. (2005). CD44 is a physiological E-selectin ligand on neutrophils. The Journal of experimental medicine, 201(8), 1183-1189. https://doi.org/10.1084/jem.20042014

Baaten, B. J. G., Tinoco, R., Chen, A. T., & Bradley, L. M. (2012). Regulation of antigen- experienced T cells: Lessons from the quintessential memory marker CD44. Frontiers in Immunology, 3, 23. https://doi.org/10.3389/fimmu.2012.00023

Naruse, M., Shibasaki, K., Yokoyama, S., Kurachi, M., & Ishizaki, Y. (2013). Dynamic changes of CD44 expression from progenitors to subpopulations of astrocytes and neurons in developing cerebellum. PloS one, 8(1), e53109. https://doi.org/10.1371/journal.pone.0053109

Liu, Y., Han, S. S., Wu, Y., Tuohy, T. M., Xue, H., Cai J., Back, S. A., Sherman, L. S., Fischer, I., & Rao, M. S. (2004). CD44 expression identifies astrocyte-restricted precursor cells. Developmental biology, 276(1), 31-46. https://doi.org/10.1016/j.ydbio.2004.08.018

Su, W., Foster, S. C., Xing, R., Feistel, K., Olsen, R. H., Acevedo, S. F., Raber, J., & Sherman, L. S. (2017). CD44 Transmembrane Receptor and Hyaluronan Regulate Adult Hippocampal Neural Stem Cell Quiescence and Differentiation. Journal of biological chemistry, 292(11), 4434-4445. https://doi.org/10.1074/jbc.M116.774109

Xie, M., Zhang, S., Dong, F., Zhang, Q., Wang, J., Wang, C., Zhu, C., Zhang, S., Luo, B., Wu, P., & Ema, H. (2021). Granulocyte colony-stimulating factor directly acts on mouse lymphoid-biased but not myeloid-biased hematopoietic stem cells. Haematologica, 106(6), 1647-1658. https://doi.org/10.3324/haematol.2019.239251

Nadar, S. K., Lip, G. Y., Lee, K. W., & Blann, A. D. (2005). Circulating endothelial cells in acute ischaemic stroke. Thrombosis and Haemostasis, 94(4), 707-712. https://doi.org/10.1160/TH04-12-0795

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Published

2023-12-05

How to Cite

1.
Kuraieva AV, Savosko SI, Grabovoy OM, Makarenko OM. Granulocyte colony-stimulating factor induces the migration of non-resident cells to intracerebral hemorrhage. Zaporozhye Medical Journal [Internet]. 2023Dec.5 [cited 2024Nov.26];25(6):528-34. Available from: http://zmj.zsmu.edu.ua/article/view/287456

Issue

Vol. 25 No. 6 (2023): Zaporozhye medical journal

Section

Original research

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