Blocking Interferon {beta} Stimulates Vascular Smooth Muscle Cell Proliferation and Arteriogenesis

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2010 Aug 26

PMID 20736166

Citations 25

Authors

Stephan H Schirmer

Pieter T Bot

Joost O Fledderus

A M van der Laan

Oscar L Volger

Ulrich Laufs

Michael Bohm

Carlie J M de Vries

Anton J G Horrevoets

Jan J Piek

Imo E Hoefer

Niels van Royen

Affiliations

Soon will be listed here.

Abstract

Increased interferon (IFN)-β signaling in patients with insufficient coronary collateralization and an inhibitory effect of IFNβ on collateral artery growth in mice have been reported. The mechanisms of IFNβ-induced inhibition of arteriogenesis are unknown. In stimulated monocytes from patients with chronic total coronary artery occlusion and decreased arteriogenic response, whole genome expression analysis showed increased expression of IFNβ-regulated genes. Immunohistochemically, the IFNβ receptor was localized in the vascular media of murine collateral arteries. Treatment of vascular smooth muscle cells (VSMC) with IFNβ resulted in an attenuated proliferation, cell-cycle arrest, and increased expression of cyclin-dependent kinase inhibitor-1A (p21). The growth inhibitory effect of IFNβ was attenuated by inhibition of p21 by RNA interference. IFNβ-treated THP1 monocytes showed enhanced apoptosis. Subsequently, we tested if collateral artery growth can be stimulated by inhibition of IFNβ-signaling. RNA interference of the IFNβ receptor-1 (IFNAR1) increased VSMC proliferation, cell cycle progression, and reduced p21 gene expression. IFNβ signaling and FAS and TRAIL expression were attenuated in monocytes from IFNAR1(-/-) mice, indicating reduced monocyte apoptosis. Hindlimb perfusion restoration 1 week after femoral artery ligation was improved in IFNAR1(-/-) mice compared with wild-type mice as assessed by infusion of fluorescent microspheres. These results demonstrate that IFNβ inhibits collateral artery growth and VSMC proliferation through p21-dependent cell cycle arrest and induction of monocyte apoptosis. Inhibition of IFNβ stimulates VSMC proliferation and collateral artery growth.

Citing Articles

SerpinG1: A Novel Biomarker Associated With Poor Coronary Collateral in Patients With Stable Coronary Disease and Chronic Total Occlusion.

Chen S, Li L, Wu Z, Liu Y, Li F, Huang K J Am Heart Assoc. 2022; 11(24):e027614.

PMID: 36515245 PMC: 9798810. DOI: 10.1161/JAHA.122.027614.

Preliminary genome wide screening identifies new variants associated with coronary artery disease in Indian population.

Bhat K, Guleria V, Kumar J R, Rastogi G, Sharma V, Sharma A Am J Transl Res. 2022; 14(7):5124-5131.

PMID: 35958505 PMC: 9360888.

p38 MAPK priming boosts VSMC proliferation and arteriogenesis by promoting PGC1α-dependent mitochondrial dynamics.

Sahun-Espanol A, Clemente C, Jimenez-Loygorri J, Sierra-Filardi E, Herrera-Melle L, Gomez-Duran A Sci Rep. 2022; 12(1):5938.

PMID: 35396524 PMC: 8994030. DOI: 10.1038/s41598-022-09757-x.

The cGAS-STING signaling in cardiovascular and metabolic diseases: Future novel target option for pharmacotherapy.

Oduro P, Zheng X, Wei J, Yang Y, Wang Y, Zhang H Acta Pharm Sin B. 2022; 12(1):50-75.

PMID: 35127372 PMC: 8799861. DOI: 10.1016/j.apsb.2021.05.011.

Lack of Cell Cycle Inhibitor p21 and Low CD4 T Cell Suppression in Newborns After Exposure to IFN-β.

Jans J, Unger W, Raeven E, Simonetti E, Eleveld M, de Groot R Front Immunol. 2021; 12:652965.

PMID: 33912177 PMC: 8071872. DOI: 10.3389/fimmu.2021.652965.

References

Angiolillo A, Sgadari C, Taub D, Liao F, Farber J, Maheshwari S . Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J Exp Med. 1995; 182(1):155-62. PMC: 2192108. DOI: 10.1084/jem.182.1.155. View

Scholz D, Ito W, Fleming I, Deindl E, Sauer A, Wiesnet M . Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch. 2000; 436(3):257-70. DOI: 10.1007/s004280050039. View

Hoefer I, van Royen N, Rectenwald J, Bray E, Abouhamze Z, Moldawer L . Direct evidence for tumor necrosis factor-alpha signaling in arteriogenesis. Circulation. 2002; 105(14):1639-41. DOI: 10.1161/01.cir.0000014987.32865.8e. View

Van Weyenbergh J, Wietzerbin J, Rouillard D, Barral-Netto M, Liblau R . Treatment of multiple sclerosis patients with interferon-beta primes monocyte-derived macrophages for apoptotic cell death. J Leukoc Biol. 2001; 70(5):745-8. View

Bendjennat M, Boulaire J, Jascur T, Brickner H, Barbier V, Sarasin A . UV irradiation triggers ubiquitin-dependent degradation of p21(WAF1) to promote DNA repair. Cell. 2003; 114(5):599-610. DOI: 10.1016/j.cell.2003.08.001. View

Schaper W . Collateral circulation: past and present. Basic Res Cardiol. 2008; 104(1):5-21. PMC: 2755790. DOI: 10.1007/s00395-008-0760-x. View

Levkau B, Koyama H, Raines E, Clurman B, Herren B, Orth K . Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol Cell. 1998; 1(4):553-63. DOI: 10.1016/s1097-2765(00)80055-6. View

Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S . Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004; 5(10):R80. PMC: 545600. DOI: 10.1186/gb-2004-5-10-r80. View

Subramanian A, Tamayo P, Mootha V, Mukherjee S, Ebert B, Gillette M . Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102(43):15545-50. PMC: 1239896. DOI: 10.1073/pnas.0506580102. View

10.

Feau S, Facchinetti V, Granucci F, Citterio S, Jarrossay D, Seresini S . Dendritic cell-derived IL-2 production is regulated by IL-15 in humans and in mice. Blood. 2004; 105(2):697-702. DOI: 10.1182/blood-2004-03-1059. View

11.

Bruhl T, Heeschen C, Aicher A, Jadidi A, Haendeler J, Hoffmann J . p21Cip1 levels differentially regulate turnover of mature endothelial cells, endothelial progenitor cells, and in vivo neovascularization. Circ Res. 2004; 94(5):686-92. DOI: 10.1161/01.RES.0000119922.71855.56. View

12.

Schirmer S, Buschmann I, Jost M, Hoefer I, Grundmann S, Andert J . Differential effects of MCP-1 and leptin on collateral flow and arteriogenesis. Cardiovasc Res. 2004; 64(2):356-64. DOI: 10.1016/j.cardiores.2004.06.022. View

13.

Goossens P, Gijbels M, Zernecke A, Eijgelaar W, Vergouwe M, van der Made I . Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell Metab. 2010; 12(2):142-53. DOI: 10.1016/j.cmet.2010.06.008. View

14.

Katayama T, Nakanishi K, Nishihara H, Kamiyama N, Nakagawa T, Kamiyama T . Type I interferon prolongs cell cycle progression via p21WAF1/CIP1 induction in human colon cancer cells. Int J Oncol. 2007; 31(3):613-20. View

15.

Celletti F, WAUGH J, Amabile P, Brendolan A, Hilfiker P, Dake M . Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med. 2001; 7(4):425-9. DOI: 10.1038/86490. View

16.

El-Deiry W, Tokino T, Velculescu V, Levy D, Parsons R, Trent J . WAF1, a potential mediator of p53 tumor suppression. Cell. 1993; 75(4):817-25. DOI: 10.1016/0092-8674(93)90500-p. View

17.

Ehrlich S, Infante-Duarte C, Seeger B, Zipp F . Regulation of soluble and surface-bound TRAIL in human T cells, B cells, and monocytes. Cytokine. 2003; 24(6):244-53. DOI: 10.1016/s1043-4666(03)00094-2. View

18.

Oehadian A, Koide N, Mu M, Hassan F, Islam S, Yoshida T . Interferon (IFN)-beta induces apoptotic cell death in DHL-4 diffuse large B cell lymphoma cells through tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Cancer Lett. 2005; 225(1):85-92. DOI: 10.1016/j.canlet.2004.11.054. View

19.

Muller U, Steinhoff U, Reis L, Hemmi S, Pavlovic J, Zinkernagel R . Functional role of type I and type II interferons in antiviral defense. Science. 1994; 264(5167):1918-21. DOI: 10.1126/science.8009221. View

20.

Zhang L, Velichko S, Vincelette J, Fitch R, Vergona R, Sullivan M . Interferon-beta attenuates angiotensin II-accelerated atherosclerosis and vascular remodeling in apolipoprotein E deficient mice. Atherosclerosis. 2007; 197(1):204-11. DOI: 10.1016/j.atherosclerosis.2007.03.019. View