Complement MASP-1 Modifies Endothelial Wound Healing

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Apr 13

PMID 38612857

Authors

Zsuzsanna Nemeth

Flora Demeter

Jozsef Dobo

Peter Gal

Laszlo Cervenak

Affiliations

Soon will be listed here.

Abstract

Endothelial wound-healing processes are fundamental for the maintenance and restoration of the circulatory system and are greatly affected by the factors present in the blood. We have previously shown that the complement protein mannan-binding lectin-associated serine protease-1 (MASP-1) induces the proinflammatory activation of endothelial cells and is able to cooperate with other proinflammatory activators. Our aim was to investigate the combined effect of mechanical wounding and MASP-1 on endothelial cells. Transcriptomic analysis showed that MASP-1 alters the expression of wound-healing-related and angiogenesis-related genes. Both wounding and MASP-1 induced Ca mobilization when applied individually. However, MASP-1-induced Ca mobilization was inhibited when the treatment was preceded by wounding. Mechanical wounding promoted CREB phosphorylation, and the presence of MASP-1 enhanced this effect. Wounding induced ICAM-1 and VCAM-1 expression on endothelial cells, and MASP-1 pretreatment further increased VCAM-1 levels. MASP-1 played a role in the subsequent stages of angiogenesis, facilitating the breakdown of the endothelial capillary network on Matrigel. Our findings extend our general understanding of endothelial wound healing and highlight the importance of complement MASP-1 activation in wound-healing processes.

References

Connolly A, Suh D, Hunt T, Coughlin S . Mice lacking the thrombin receptor, PAR1, have normal skin wound healing. Am J Pathol. 1997; 151(5):1199-204. PMC: 1858088. View

Dhondt C, Ponsaerts R, Srinivas S, Vereecke J, Himpens B . Reduced intercellular communication and altered morphology of bovine corneal endothelial cells with prolonged time in cell culture. Curr Eye Res. 2009; 34(6):454-65. DOI: 10.1080/02713680902913022. View

OBrien K, Allen M, McDonald T, Chait A, Harlan J, Fishbein D . Vascular cell adhesion molecule-1 is expressed in human coronary atherosclerotic plaques. Implications for the mode of progression of advanced coronary atherosclerosis. J Clin Invest. 1993; 92(2):945-51. PMC: 294934. DOI: 10.1172/JCI116670. View

van der LAAN N, de Leij L, Ten Duis H . Immunohistopathological appearance of three different types of injury in human skin. Inflamm Res. 2001; 50(7):350-6. DOI: 10.1007/PL00000255. View

Chan B, Merchan J, Kale S, Sukhatme V . Antiangiogenic property of human thrombin. Microvasc Res. 2003; 66(1):1-14. DOI: 10.1016/s0026-2862(03)00037-2. View

Garred P, Genster N, Pilely K, Bayarri-Olmos R, Rosbjerg A, Ma Y . A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev. 2016; 274(1):74-97. DOI: 10.1111/imr.12468. View

Debreczeni M, Nemeth Z, Kajdacsi E, Schwaner E, Mako V, Masszi A . MASP-1 Increases Endothelial Permeability. Front Immunol. 2019; 10:991. PMC: 6509239. DOI: 10.3389/fimmu.2019.00991. View

Schwaner E, Nemeth Z, Jani P, Kajdacsi E, Debreczeni M, Doleschall Z . Transcriptome analysis of inflammation-related gene expression in endothelial cells activated by complement MASP-1. Sci Rep. 2017; 7(1):10462. PMC: 5585174. DOI: 10.1038/s41598-017-09058-8. View

Jordan J, Montalto M, Stahl G . Inhibition of mannose-binding lectin reduces postischemic myocardial reperfusion injury. Circulation. 2001; 104(12):1413-8. DOI: 10.1161/hc3601.095578. View

10.

Korkmaz H, Krijnen P, Ulrich M, de Jong E, van Zuijlen P, Niessen H . The role of complement in the acute phase response after burns. Burns. 2017; 43(7):1390-1399. DOI: 10.1016/j.burns.2017.03.007. View

11.

Demeter F, Nemeth Z, Kajdacsi E, Bihari G, Dobo J, Gal P . Detrimental interactions of hypoxia and complement MASP-1 in endothelial cells as a model for atherosclerosis-related diseases. Sci Rep. 2024; 14(1):14882. PMC: 11211410. DOI: 10.1038/s41598-024-64479-6. View

12.

Demer L, Wortham C, DIRKSEN E, Sanderson M . Mechanical stimulation induces intercellular calcium signaling in bovine aortic endothelial cells. Am J Physiol. 1993; 264(6 Pt 2):H2094-102. DOI: 10.1152/ajpheart.1993.264.6.H2094. View

13.

Sinno H, Prakash S . Complements and the wound healing cascade: an updated review. Plast Surg Int. 2013; 2013:146764. PMC: 3741993. DOI: 10.1155/2013/146764. View

14.

Nemeth Z, Debreczeni M, Kajdacsi E, Dobo J, Gal P, Cervenak L . Cooperation of Complement MASP-1 with Other Proinflammatory Factors to Enhance the Activation of Endothelial Cells. Int J Mol Sci. 2023; 24(11). PMC: 10252236. DOI: 10.3390/ijms24119181. View

15.

Megyeri M, Mako V, Beinrohr L, Doleschall Z, Prohaszka Z, Cervenak L . Complement protease MASP-1 activates human endothelial cells: PAR4 activation is a link between complement and endothelial function. J Immunol. 2009; 183(5):3409-16. DOI: 10.4049/jimmunol.0900879. View

16.

Megyeri M, Harmat V, Major B, Vegh A, Balczer J, Heja D . Quantitative characterization of the activation steps of mannan-binding lectin (MBL)-associated serine proteases (MASPs) points to the central role of MASP-1 in the initiation of the complement lectin pathway. J Biol Chem. 2013; 288(13):8922-34. PMC: 3610966. DOI: 10.1074/jbc.M112.446500. View

17.

Huber-Lang M, Ignatius A, Kohl J, Mannes M, Braun C . Complement in trauma-Traumatised complement?. Br J Pharmacol. 2020; 178(14):2863-2879. DOI: 10.1111/bph.15245. View

18.

Fumagalli S, Perego C, Zangari R, De Blasio D, Oggioni M, De Nigris F . Lectin Pathway of Complement Activation Is Associated with Vulnerability of Atherosclerotic Plaques. Front Immunol. 2017; 8:288. PMC: 5352714. DOI: 10.3389/fimmu.2017.00288. View

19.

Tsirogianni A, Moutsopoulos N, Moutsopoulos H . Wound healing: immunological aspects. Injury. 2006; 37 Suppl 1:S5-12. DOI: 10.1016/j.injury.2006.02.035. View

20.

Kameritsch P, Pogoda K, Ritter A, Munzing S, Pohl U . Gap junctional communication controls the overall endothelial calcium response to vasoactive agonists. Cardiovasc Res. 2011; 93(3):508-15. DOI: 10.1093/cvr/cvr345. View