Microvesicles produced by monocytes affect the phenotype and functions of endothelial cells

Dmitriy I. Sokolov; Anastasia R. Kozyreva; Kseniia L. Markova; Valentina A. Mikhailova; Andrey V. Korenevskii; Yulia P. Miliutina; Olga A. Balabas; Sergey V. Chepanov; Sergey A. Selkov; Dmitriy I. Sokolov; Anastasia R. Kozyreva; Kseniia L. Markova; Valentina A. Mikhailova; Andrey V. Korenevskii; Yulia P. Miliutina; Olga A. Balabas; Sergey V. Chepanov; Sergey A. Selkov

doi:10.3934/Allergy.2021011

AIMS Allergy and Immunology

2021, Volume 5, Issue 3: 135-159. doi: 10.3934/Allergy.2021011

Previous Article Next Article

Research article Special Issues

Microvesicles produced by monocytes affect the phenotype and functions of endothelial cells

1.
Federal State Budgetary Scientific Institution, Research Institute of Obstetrics, Gynecology, and Reproductology named after D.O. Ott, Saint Petersburg, Russia
2.
Chemical Analysis and Materials Research Centre, Federal State Budgetary Educational Institution of Higher Education, Saint Petersburg State University, Saint Petersburg, Russia

Received: 26 March 2021 Accepted: 10 May 2021 Published: 14 May 2021

Monocytes\macrophages regulate angiogenesis via cytokine production and contact interactions with endothelial cells (ECs). The biological effects of macrophage-derived microvesicles (MVs) are studied using cell lines, such as monocytic leukemia THP-1 cell line. The effect of MVs produced by THP-1 cells on EC phenotype and functions remain understudied. In this research, we studied the effect of MVs produced by THP-1 cells on the phenotype, proliferation, migration, and vascular formation of EA.Hy926 ECs. MVs produced by THP-1 cells express CD54, CD18, CD11a, CD11b, CD29, CD120a, CD120b, VEGFR1, VEGFR2, CD105, CD119, TGFR2 on the surface and contain ERK1/2, pERK1/2 Akt, FGF10, endothelin-2. The transfer of an intracellular protein labeled with a fluorescent dye from MVs produced by THP-1 cells to EA.Hy926 ECs was established. It was found that MVs derived from THP-1 cells inhibit EC proliferation. In high concentrations, MVs reduce EC migration, increase the length but decrease the number of vessels formed by ECs, promoting the development of non-branching angiogenesis. On the contrary, in low concentrations, MVs increase EC migration, reduce the length, and increase the number of vessels formed by ECs, promoting the development of branching angiogenesis. Thus, the fundamental possibility of the influence of MVs produced by THP-1 cells on the processes of angiogenesis has been established. Proteins found in the MVs composition may be responsible for the observed effects of MVs on ECs.
- monocytes,
- macrophages,
- endothelium,
- microvesicles,
- proliferation,
- migration,
- angiogenesis, endoglin,
- TGFβ,
- FGF10
Citation: Dmitriy I. Sokolov, Anastasia R. Kozyreva, Kseniia L. Markova, Valentina A. Mikhailova, Andrey V. Korenevskii, Yulia P. Miliutina, Olga A. Balabas, Sergey V. Chepanov, Sergey A. Selkov. Microvesicles produced by monocytes affect the phenotype and functions of endothelial cells[J]. AIMS Allergy and Immunology, 2021, 5(3): 135-159. doi: 10.3934/Allergy.2021011

Related Papers:

Abstract

Monocytes\macrophages regulate angiogenesis via cytokine production and contact interactions with endothelial cells (ECs). The biological effects of macrophage-derived microvesicles (MVs) are studied using cell lines, such as monocytic leukemia THP-1 cell line. The effect of MVs produced by THP-1 cells on EC phenotype and functions remain understudied. In this research, we studied the effect of MVs produced by THP-1 cells on the phenotype, proliferation, migration, and vascular formation of EA.Hy926 ECs. MVs produced by THP-1 cells express CD54, CD18, CD11a, CD11b, CD29, CD120a, CD120b, VEGFR1, VEGFR2, CD105, CD119, TGFR2 on the surface and contain ERK1/2, pERK1/2 Akt, FGF10, endothelin-2. The transfer of an intracellular protein labeled with a fluorescent dye from MVs produced by THP-1 cells to EA.Hy926 ECs was established. It was found that MVs derived from THP-1 cells inhibit EC proliferation. In high concentrations, MVs reduce EC migration, increase the length but decrease the number of vessels formed by ECs, promoting the development of non-branching angiogenesis. On the contrary, in low concentrations, MVs increase EC migration, reduce the length, and increase the number of vessels formed by ECs, promoting the development of branching angiogenesis. Thus, the fundamental possibility of the influence of MVs produced by THP-1 cells on the processes of angiogenesis has been established. Proteins found in the MVs composition may be responsible for the observed effects of MVs on ECs.

Abbreviations

ECs

endothelial cells

MVs

microvesicles

ECM

extracellular matrix

MMPs

metalloproteinases

IQR

interquartile range

CFSE

carboxyfluorescein diacetate succinimidyl ester

MFI

mean fluorescence intensity

Acknowledgments

The authors thank V.A. Semyonov for assistance in managing cell cultures. The study was supported by AAAA-A19-119021290116-1 (cell line culturing). Phenotyping of THP-1 cells and their MVs, assessment of proliferation, migration, and vascular tube formation, WesternBlot and MALDI-TOF-mass spectrometry analysis was supported by RFBR grant No. 19-015-00218. Participation of A.R. Kozyreva was supported by the scholarship of the President of the Russian Federation SP-420.2019.4. The funders did not participate in the design, data collection or analysis of this research, or preparation or publication of this manuscript. Mass spectrometry analysis was performed in the Chemical Analysis and Materials Research Centre of the Federal State Budgetary Educational Institution of Higher Education: Saint Petersburg State University, Saint Petersburg, Russia.

Conflict of interest

All authors declare no conflicts of interest in this paper.

References

[1]	Bingle L, Lewis CE, Corke KP, et al. (2006) Macrophages promote angiogenesis in human breast tumour spheroids in vivo. Brit J Cancer 94: 101-107. doi: 10.1038/sj.bjc.6602901
[2]	Riabov V, Gudima A, Wang N, et al. (2014) Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front Physiol 5: 75. doi: 10.3389/fphys.2014.00075
[3]	Fantin A, Vieira JM, Gestri G, et al. (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116: 829-840. doi: 10.1182/blood-2009-12-257832
[4]	Schmidt T, Carmeliet P (2010) Blood-vessel formation: Bridges that guide and unite. Nature 465: 697-699. doi: 10.1038/465697a
[5]	Olivo M, Bhardwaj R, Schulze-Osthoff K, et al. (1992) A comparative study on the effects of tumor necrosis factor-alpha (TNF-alpha), human angiogenic factor (h-AF) and basic fibroblast growth factor (bFGF) on the chorioallantoic membrane of the chick embryo. Anat Rec 234: 105-115. doi: 10.1002/ar.1092340112
[6]	Sunderkotter C, Goebeler M, Schulze-Osthoff K, et al. (1991) Macrophage-derived angiogenesis factors. Pharmacol Therapeut 51: 195-216. doi: 10.1016/0163-7258(91)90077-Y
[7]	Hockel M, Sasse J, Wissler JH (1987) Purified monocyte-derived angiogenic substance (angiotropin) stimulates migration, phenotypic changes, and “tube formation” but not proliferation of capillary endothelial cells in vitro. J Cell Physiol 133: 1-13. doi: 10.1002/jcp.1041330102
[8]	Chen J, Wang Z, Zheng Z, et al. (2017) Neuron and microglia/macrophage-derived FGF10 activate neuronal FGFR2/PI3K/Akt signaling and inhibit microglia/macrophages TLR4/NF-kappaB-dependent neuroinflammation to improve functional recovery after spinal cord injury. Cell Death Discov 8: e3090. doi: 10.1038/cddis.2017.490
[9]	Wynn TA, Barron L (2010) Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 30: 245-257. doi: 10.1055/s-0030-1255354
[10]	Liu HM, Wang DL, Liu CY (1990) Interactions between fibrin, collagen and endothelial cells in angiogenesis. Adv Exp Med Biol 281: 319-331. doi: 10.1007/978-1-4615-3806-6_34
[11]	Ismail N, Wang Y, Dakhlallah D, et al. (2013) Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 121: 984-995. doi: 10.1182/blood-2011-08-374793
[12]	Tricarico C, Clancy J, D'Souza-Schorey C (2017) Biology and biogenesis of shed microvesicles. Small GTPases 8: 220-232. doi: 10.1080/21541248.2016.1215283
[13]	Obregon C, Rothen-Rutishauser B, Gerber P, et al. (2009) Active uptake of dendritic cell-derived exovesicles by epithelial cells induces the release of inflammatory mediators through a TNF-alpha-mediated pathway. Am J Pathol 175: 696-705. doi: 10.2353/ajpath.2009.080716
[14]	Muralidharan-Chari V, Clancy J, Plou C, et al. (2009) ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 19: 1875-1885. doi: 10.1016/j.cub.2009.09.059
[15]	Wang T, Gilkes DM, Takano N, et al. (2014) Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. P Natl Acad Sci USA 111: E3234-E 3242. doi: 10.1073/pnas.1410041111
[16]	Martinez de Lizarrondo S, Roncal C, Calvayrac O, et al. (2012) Synergistic effect of thrombin and CD40 ligand on endothelial matrix metalloproteinase-10 expression and microparticle generation in vitro and in vivo. Arterioscl Throm Vas 32: 1477-1487. doi: 10.1161/ATVBAHA.112.248773
[17]	Li CJ, Liu Y, Chen Y, et al. (2013) Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke. Am J Pathol 182: 1552-1562. doi: 10.1016/j.ajpath.2013.01.035
[18]	Mochizuki S, Okada Y (2007) ADAMs in cancer cell proliferation and progression. Cancer Sci 98: 621-628. doi: 10.1111/j.1349-7006.2007.00434.x
[19]	Mezouar S, Darbousset R, Dignat-George F, et al. (2015) Inhibition of platelet activation prevents the P-selectin and integrin-dependent accumulation of cancer cell microparticles and reduces tumor growth and metastasis in vivo. Int J Cancer 136: 462-475. doi: 10.1002/ijc.28997
[20]	Falati S, Liu Q, Gross P, et al. (2003) Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 197: 1585-1598. doi: 10.1084/jem.20021868
[21]	Del Conde I, Shrimpton CN, Thiagarajan P, et al. (2005) Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106: 1604-1611. doi: 10.1182/blood-2004-03-1095
[22]	Pluskota E, Woody NM, Szpak D, et al. (2008) Expression, activation, and function of integrin α_Mβ₂ (Mac-1) on neutrophil-derived microparticles. Blood 112: 2327-2335. doi: 10.1182/blood-2007-12-127183
[23]	Garzetti L, Menon R, Finardi A, et al. (2014) Activated macrophages release microvesicles containing polarized M1 or M2 mRNAs. J Leukocyte Biol 95: 817-825. doi: 10.1189/jlb.0913485
[24]	Ward JR, West PW, Ariaans MP, et al. (2010) Temporal interleukin-1beta secretion from primary human peripheral blood monocytes by P2X7-independent and P2X7-dependent mechanisms. J Biol Chem 285: 23147-23158. doi: 10.1074/jbc.M109.072793
[25]	Zhang Y, Liu D, Chen X, et al. (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39: 133-144. doi: 10.1016/j.molcel.2010.06.010
[26]	Aras O, Shet A, Bach RR, et al. (2004) Induction of microparticle- and cell-associated intravascular tissue factor in human endotoxemia. Blood 103: 4545-4553. doi: 10.1182/blood-2003-03-0713
[27]	Nguyen MA, Karunakaran D, Geoffrion M, et al. (2018) Extracellular vesicles secreted by atherogenic macrophages transfer microRNA to inhibit cell migration. Arterioscl Throm Vas 38: 49-63. doi: 10.1161/ATVBAHA.117.309795
[28]	Soni S, Wilson MR, O'Dea KP, et al. (2016) Alveolar macrophage-derived microvesicles mediate acute lung injury. Thorax 71: 1020-1029. doi: 10.1136/thoraxjnl-2015-208032
[29]	Edgell CJ, McDonald CC, Graham JB (1983) Permanent cell line expressing human factor VIII-related antigen established by hybridization. P Natl Acad Sci USA 80: 3734-3737. doi: 10.1073/pnas.80.12.3734
[30]	Thornhill MH, Li J, Haskard DO (1993) Leucocyte endothelial cell adhesion: a study comparing human umbilical vein endothelial cells and the endothelial cell line EA-hy-926. Scand J Immunol 38: 279-286. doi: 10.1111/j.1365-3083.1993.tb01726.x
[31]	Riesbeck K, Billstrom A, Tordsson J, et al. (1998) Endothelial cells expressing an inflammatory phenotype are lysed by superantigen-targeted cytotoxic T cells. Clin Diagn Lab Immun 5: 675-682. doi: 10.1128/CDLI.5.5.675-682.1998
[32]	Sokolov DI, Lvova TY, Okorokova LS, et al. (2017) Effect of cytokines on the formation tube-like structure by endothelial cells in the presence of trophoblast cells. Bull Exp Biol Med 163: 148-158. doi: 10.1007/s10517-017-3756-4
[33]	van der Pol E, Coumans FA, Grootemaat AE, et al. (2014) Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost 12: 1182-1192. doi: 10.1111/jth.12602
[34]	Xu R, Greening DW, Zhu HJ, et al. (2016) Extracellular vesicle isolation and characterization: toward clinical application. J Clin Invest 126: 1152-1162. doi: 10.1172/JCI81129
[35]	Li P, Kaslan M, Lee SH, et al. (2017) Progress in Exosome Isolation Techniques. Theranostics 7: 789-804. doi: 10.7150/thno.18133
[36]	Simak J, Gelderman MP, Yu H, et al. (2006) Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J Thromb Haemost 4: 1296-1302. doi: 10.1111/j.1538-7836.2006.01911.x
[37]	Sokolov DI, Ovchinnikova OM, Korenkov DA, et al. (2016) Influence of peripheral blood microparticles of pregnant women with preeclampsia on the phenotype of monocytes. Transl Res 170: 112-123. doi: 10.1016/j.trsl.2014.11.009
[38]	Sokolov DI, Markova KL, Mikhailova VA, et al. (2019) Phenotypic and functional characteristics of microvesicles produced by natural killer cells. Med Immunol (Russia) 21: 669-688. doi: 10.15789/1563-0625-2019-4-669-688
[39]	Korenevskii AV, Milyutina YP, Zhdanova AA, et al. (2018) Mass-Spectrometric Analysis of Proteome of Microvesicles Produced by NK-92 Natural Killer Cells. B Exp Biol Med+ 165: 564-571. doi: 10.1007/s10517-018-4214-7
[40]	Evans-Osses I, Reichembach LH, Ramirez MI (2015) Exosomes or microvesicles? Two kinds of extracellular vesicles with different routes to modify protozoan-host cell interaction. Parasitol Res 114: 3567-3575. doi: 10.1007/s00436-015-4659-9
[41]	Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254. doi: 10.1016/0003-2697(76)90527-3
[42]	Mikhailova VA, Belyakova KL, Vyazmina LP, et al. (2018) Evaluation of microvesicles formed by natural killer (Nk) cells using flow cytometry. Med Immunol (Russia) 20: 251-254. doi: 10.15789/1563-0625-2018-2-251-254
[43]	Markova KL, Mikhailova VA, Korenevsky AV, et al. (2020) Microvesicles produced by natural killer cells of the NK-92 cell line affect the phenotype and functions of endothelial cells of the EA.Hy926 cell line. Med Immunol (Russia) 22: 249-268. doi: 10.15789/1563-0625-MPB-1877
[44]	Sokolov DI, Furaeva KN, Stepanova OI, et al. (2015) Proliferative and migration activity of JEG-3 trophoblast cell line in the presence of cytokines. B Exp Biol Med+ 159: 550-556. doi: 10.1007/s10517-015-3013-7
[45]	Markov AS, Markova KL, Sokolov DI, et al. Registration certificate No. 2019612366 for computer program “MarkMigration” (2019) .Available from:https://www.fips.ru/en/.
[46]	Gojova A, Barakat AI (2005) Vascular endothelial wound closure under shear stress: role of membrane fluidity and flow-sensitive ion channels. J Appl Physiol 98: 2355-2362. doi: 10.1152/japplphysiol.01136.2004
[47]	Si Y, Chu H, Zhu W, et al. (2018) Concentration-dependent effects of rapamycin on proliferation, migration and apoptosis of endothelial cells in human venous malformation. Exp Ther Med 16: 4595-4601.
[48]	Markova KL, Kozyreva AR, Sokolov DI, et al. (2020) Microvesicles produced by natural killer cells regulate the formation of blood vessels. B Exp Biol Med+ 170: 123-127. doi: 10.1007/s10517-020-05017-y
[49]	Ponce ML (2009) Tube formation: an in vitro matrigel angiogenesis assay. Methods Mol Biol 467: 183-188. doi: 10.1007/978-1-59745-241-0_10
[50]	Waters WR, Harkins KR, Wannemuehler MJ (2002) Five-color flow cytometric analysis of swine lymphocytes for detection of proliferation, apoptosis, viability, and phenotype. Cytometry 48: 146-152. doi: 10.1002/cyto.10122
[51]	Philpott NJ, Scopes J, Marsh JC, et al. (1995) Increased apoptosis in aplastic anemia bone marrow progenitor cells: possible pathophysiologic significance. Exp Hematol 23: 1642-1648.
[52]	Bass JJ, Wilkinson DJ, Rankin D, et al. (2017) An overview of technical considerations for Western blotting applications to physiological research. Scand J Med Sci Spor 27: 4-25. doi: 10.1111/sms.12702
[53]	Hamamura-Yasuno E, Aida T, Tsuchiya Y, et al. (2020) Immunostimulatory effects on THP-1 cells by peptide or protein pharmaceuticals associated with injection site reactions. J Immunotoxicol 17: 59-66. doi: 10.1080/1547691X.2020.1727071
[54]	Ito M, Yamamoto T, Watanabe M, et al. (1996) Detection of measles virus-induced apoptosis of human monocytic cell line (THP-1) by DNA fragmentation ELISA. FEMS Immunol Med Mic 15: 115-122. doi: 10.1111/j.1574-695X.1996.tb00061.x
[55]	Manna P, Jain SK (2014) Effect of PIP3 on adhesion molecules and adhesion of THP-1 monocytes to HUVEC treated with high glucose. Cell Physiol Biochem 33: 1197-1204. doi: 10.1159/000358688
[56]	Zhang X, Shang W, Yuan J, et al. (2016) Positive feedback cycle of TNFalpha promotes staphylococcal enterotoxin B-induced THP-1 cell apoptosis. Front Cell Infect Microbiol 6: 109.
[57]	Arjuman A, Chandra NC (2015) Differential pro-inflammatory responses of TNF-alpha receptors (TNFR1 and TNFR2) on LOX-1 signalling. Mol Biol Rep 42: 1039-1047. doi: 10.1007/s11033-014-3841-y
[58]	Spiekermann K, Faber F, Voswinckel R, et al. (2002) The protein tyrosine kinase inhibitor SU5614 inhibits VEGF-induced endothelial cell sprouting and induces growth arrest and apoptosis by inhibition of c-kit in AML cells. Exp Hematol 30: 767-773. doi: 10.1016/S0301-472X(02)00837-8
[59]	Ligi D, Croce L, Mosti G, et al. (2017) Chronic venous insufficiency: transforming growth factor-β isoforms and soluble endoglin concentration in different states of wound healing. Int J Mol Sci 18: 2206. doi: 10.3390/ijms18102206
[60]	Li X, O'Regan AW, Berman JS (2003) IFN-gamma induction of osteopontin expression in human monocytoid cells. J Interf Cytok Res 23: 259-265. doi: 10.1089/107999003321829971
[61]	Liu JH, Wei S, Burnette PK, et al. (1999) Functional association of TGF-beta receptor II with cyclin B. Oncogene 18: 269-275. doi: 10.1038/sj.onc.1202263
[62]	Huang Y, Tian C, Li Q, et al. (2019) TET1 knockdown inhibits Porphyromonas gingivalis LPS/IFN-γ-induced M1 macrophage polarization through the NF-κB pathway in THP-1 cells. Int J Mol Sci 20: 2023. doi: 10.3390/ijms20082023
[63]	Chen RF, Wang L, Cheng JT, et al. (2012) Induction of IFNalpha or IL-12 depends on differentiation of THP-1 cells in dengue infections without and with antibody enhancement. BMC Infect Dis 12: 340. doi: 10.1186/1471-2334-12-340
[64]	Barker KS, Liu T, Rogers PD (2005) Coculture of THP-1 human mononuclear cells with Candida albicans results in pronounced changes in host gene expression. J Infect Dis 192: 901-912. doi: 10.1086/432487
[65]	Groh L, Keating ST, Joosten LAB, et al. (2018) Monocyte and macrophage immunometabolism in atherosclerosis. Semin Immunopathol 40: 203-214. doi: 10.1007/s00281-017-0656-7
[66]	Chrobok NL, Sestito C, Wilhelmus MM, et al. (2017) Is monocyte- and macrophage-derived tissue transglutaminase involved in inflammatory processes? Amino Acids 49: 441-452. doi: 10.1007/s00726-016-2334-9
[67]	Dalton HJ, Armaiz-Pena GN, Gonzalez-Villasana V, et al. (2014) Monocyte subpopulations in angiogenesis. Cancer Res 74: 1287-1293. doi: 10.1158/0008-5472.CAN-13-2825
[68]	Laviv Y, Kasper B, Kasper EM (2018) Vascular hyperpermeability as a hallmark of phacomatoses: is the etiology angiogenesis related to or comparable with mechanisms seen in inflammatory pathways? Part II: angiogenesis- and inflammation-related molecular pathways, tumor-associated macrophages, and possible therapeutic implications: a comprehensive review. Neurosurg Rev 41: 931-944. doi: 10.1007/s10143-017-0837-9
[69]	Andreu Z, Yanez-Mo M (2014) Tetraspanins in extracellular vesicle formation and function. Front Immunol 5: 442. doi: 10.3389/fimmu.2014.00442
[70]	Colombo M, Raposo G, Thery C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Bi 30: 255-289. doi: 10.1146/annurev-cellbio-101512-122326
[71]	Hemler ME (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Bi 19: 397-422. doi: 10.1146/annurev.cellbio.19.111301.153609
[72]	Kalucka J, Bierhansl L, Wielockx B, et al. (2017) Interaction of endothelial cells with macrophages-linking molecular and metabolic signaling. Pflug Arch Eur J Phy 469: 473-483. doi: 10.1007/s00424-017-1946-6
[73]	Levine SJ (2008) Molecular mechanisms of soluble cytokine receptor generation. J Biol Chem 283: 14177-14181. doi: 10.1074/jbc.R700052200
[74]	Sedgwick AE, D'Souza-Schorey C (2018) The biology of extracellular microvesicles. Traffic 19: 319-327. doi: 10.1111/tra.12558
[75]	Mulcahy LA, Pink RC, Carter DR (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 3: 24641. doi: 10.3402/jev.v3.24641
[76]	Rozmyslowicz T, Majka M, Kijowski J, et al. (2003) Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS 17: 33-42. doi: 10.1097/00002030-200301030-00006
[77]	Christianson HC, Svensson KJ, van Kuppevelt TH, et al. (2013) Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. P Natl Acad Sci USA 110: 17380-17385. doi: 10.1073/pnas.1304266110
[78]	Keskin U, Ulubay M, Dede M, et al. (2015) The relationship between the VEGF/sVEGFR-1 ratio and threatened abortion. Arch Gynecol Obstet 291: 557-561. doi: 10.1007/s00404-014-3452-9
[79]	Guan XJ, Song L, Han FF, et al. (2013) Mesenchymal stem cells protect cigarette smoke-damaged lung and pulmonary function partly via VEGF-VEGF receptors. J Cell Biochem 114: 323-335. doi: 10.1002/jcb.24377
[80]	Guerra A, Belinha J, Mangir N, et al. (2020) Sprouting angiogenesis: A numerical approach with experimental validation. Ann Biomed Eng 49: 871-884. doi: 10.1007/s10439-020-02622-w
[81]	Hellbach N, Weise SC, Vezzali R, et al. (2014) Neural deletion of Tgfbr2 impairs angiogenesis through an altered secretome. Hum Mol Genet 23: 6177-6190. doi: 10.1093/hmg/ddu338
[82]	Gallardo-Vara E, Tual-Chalot S, Botella LM, et al. (2018) Soluble endoglin regulates expression of angiogenesis-related proteins and induction of arteriovenous malformations in a mouse model of hereditary hemorrhagic telangiectasia. Dis Models Mech 11: dmm034397. doi: 10.1242/dmm.034397
[83]	Pan CC, Bloodworth JC, Mythreye K, et al. (2012) Endoglin inhibits ERK-induced c-Myc and cyclin D1 expression to impede endothelial cell proliferation. Biochem Bioph Res Co 424: 620-623. doi: 10.1016/j.bbrc.2012.06.163
[84]	Roman AC, Carvajal-Gonzalez JM, Rico-Leo EM, et al. (2009) Dioxin receptor deficiency impairs angiogenesis by a mechanism involving VEGF-A depletion in the endothelium and transforming growth factor-beta overexpression in the stroma. J Biol Chem 284: 25135-25148. doi: 10.1074/jbc.M109.013292
[85]	Ling L, Maguire JJ, Davenport AP (2013) Endothelin-2, the forgotten isoform: emerging role in the cardiovascular system, ovarian development, immunology and cancer. Brit J Pharmacol 168: 283-295. doi: 10.1111/j.1476-5381.2011.01786.x
[86]	Lankhorst S, Danser AH, van den Meiracker AH (2016) Endothelin-1 and antiangiogenesis. Am J Physiol-Reg I 310: R230-R234.
[87]	Kandalaft LE, Motz GT, Busch J, et al. (2010) Angiogenesis and the tumor vasculature as antitumor immune modulators: the role of vascular endothelial growth factor and endothelin. Cancer Immunol Immunother 344: 129-148. doi: 10.1007/82_2010_95
[88]	Sugimoto K, Yoshida S, Mashio Y, et al. (2014) Role of FGF10 on tumorigenesis by MS-K. Genes Cells 19: 112-125. doi: 10.1111/gtc.12118
[89]	Walker DJ, Land SC (2018) Regulation of vascular signalling by nuclear Sprouty2 in fetal lung epithelial cells: Implications for co-ordinated airway and vascular branching in lung development. Comp Biochem Phys B 224: 105-114. doi: 10.1016/j.cbpb.2018.01.007
[90]	Hui Q, Jin Z, Li X, et al. (2018) FGF family: from drug development to clinical application. Int J Mol Sci 19: 1875. doi: 10.3390/ijms19071875
[91]	Maretzky T, Evers A, Zhou W, et al. (2011) Migration of growth factor-stimulated epithelial and endothelial cells depends on EGFR transactivation by ADAM17. Nat Commun 2: 229. doi: 10.1038/ncomms1232
[92]	Chen P, Zhang H, Zhang Q, et al. (2019) basic fibroblast growth factor reduces permeability and apoptosis of human brain microvascular endothelial cells in response to oxygen and glucose deprivation followed by reoxygenation via the fibroblast growth factor receptor 1 (FGFR1)/ERK pathway. Med Sci Monit 25: 7191-7201. doi: 10.12659/MSM.918626
[93]	Winter SF, Acevedo VD, Gangula RD, et al. (2007) Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2. Oncogene 26: 4897-4907. doi: 10.1038/sj.onc.1210288
[94]	Parsons-Wingerter P, Elliott KE, Clark JI, et al. (2000) Fibroblast growth factor-2 selectively stimulates angiogenesis of small vessels in arterial tree. Arterioscl Throm Vas 20: 1250-1256. doi: 10.1161/01.ATV.20.5.1250
[95]	Katoh M, Nakagama H (2014) FGF receptors: cancer biology and therapeutics. Med Res Rev 34: 280-300. doi: 10.1002/med.21288
[96]	Siqueira M, Francis D, Gisbert D, et al. (2018) Radial glia cells control angiogenesis in the developing cerebral cortex through TGF-beta1 signaling. Mol Neurobiol 55: 3660-3675.
[97]	ten Dijke P, Arthur HM (2007) Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Bio 8: 857-869. doi: 10.1038/nrm2262
[98]	Ding W, Shi W, Bellusci S, et al. (2007) Sprouty2 downregulation plays a pivotal role in mediating crosstalk between TGF-beta1 signaling and EGF as well as FGF receptor tyrosine kinase-ERK pathways in mesenchymal cells. J Cell Physiol 212: 796-806. doi: 10.1002/jcp.21078

allergy-05-03-011-s001.pdf

Reader Comments

Your name:*

Email:*
© 2021 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)