Abstract
Intracranial aneurysms (IA) are a huge threat to human health, with a global incidence rate of 0.65–8.4%. Although the microsurgical and interventional techniques have made profound progression in treating IA, the relatively high rate of complications and recurrence are still not satisfactory. Thus, there is a need to elucidate its molecular mechanism. Numerous studies have identified the close relationship between hemodynamic-induced inflammation and development of IA. Indeed, the dysfunction of endothelial cells, smooth muscle cells, macrophages and lymphocytes, as well as their secreted cytokines, collectively contribute to the formation, growth and rupture of IA. Furthermore, the immune system has also been identified to participate in the development of IA. This review will explore the mechanisms of various inflammatory cells and significant cytokines, providing a new perspective in the clinical treatment of IA.
Keywords: Hemodynamic, intracranial aneurysm, inflammation, cytokines, endothelial cells, cytokines.
Graphical Abstract
[1]
Li, M.H.; Chen, S.W.; Li, Y.D.; Chen, Y.C.; Cheng, Y.S.; Hu, D.J.; Tan, H.Q.; Wu, Q.; Wang, W.; Sun, Z.K.; Wei, X.E.; Zhang, J.Y.; Qiao, R.H.; Zong, W.H.; Zhang, Y.; Lou, W.; Chen, Z.Y.; Zhu, Y.; Peng, D.R.; Ding, S.X.; Xu, X.F.; Hou, X.H.; Jia, W.P. Prevalence of unruptured cerebral aneurysms in Chinese adults aged 35 to 75 years: A cross-sectional study. Ann. Intern. Med., 2013, 159(8), 514-521.
[2]
Li, J.; Shen, B.; Ma, C.; Liu, L.; Ren, L.; Fang, Y.; Dai, D.; Chen, S.; Lu, J. 3D contrast enhancement-MR angiography for imaging of unruptured cerebral aneurysms: a hospital-based prevalence study. PLoS One, 2014, 9(12), e114157.
[3]
(a) Morita, A.; Kirino, T.; Hashi, K.; Aoki, N.; Fukuhara, S.; Hashimoto, N.; Nakayama, T.; Sakai, M.; Teramoto, A.; Tominari, S.; Yoshimoto, T. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N. Engl. J. Med., 2012, 366(26), 2474-2482.
(b) Winn, H.R.; Britz, G.W. Unruptured aneurysms. J. Neurosurg., 2006, 104(2), 179-180.
(c) Vlak, M.H.; Algra, A.; Brandenburg, R.; Rinkel, G.J. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: A systematic review and meta-analysis. Lancet Neurol., 2011, 10(7), 626-636.
(b) Winn, H.R.; Britz, G.W. Unruptured aneurysms. J. Neurosurg., 2006, 104(2), 179-180.
(c) Vlak, M.H.; Algra, A.; Brandenburg, R.; Rinkel, G.J. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: A systematic review and meta-analysis. Lancet Neurol., 2011, 10(7), 626-636.
[5]
van Gijn, J.; Kerr, R.S.; Rinkel, G.J. Subarachnoid haemorrhage. Lancet, 2007, 369(9558), 306-318.
[6]
(a) Schievink, W.I. Intracranial aneurysms. N. Engl. J. Med., 1997, 336(1), 28-40.
(b) Chalouhi, N.; Chitale, R.; Jabbour, P.; Tjoumakaris, S.; Dumont, A.S.; Rosenwasser, R.; Gonzalez, L.F. The case for family screening for intracranial aneurysms. Neurosurg. Focus, 2011, 31(6), E8.
(c) Kang, H.; Peng, T.; Qian, Z.; Li, Y.; Jiang, C.; Ji, W.; Wu, J.; Xu, W.; Wen, X.; Liu, A. Impact of hypertension and smoking on the rupture of intracranial aneurysms and their joint effect. Neurol. Neurochir. Pol., 2015, 49(2), 121-125.
(b) Chalouhi, N.; Chitale, R.; Jabbour, P.; Tjoumakaris, S.; Dumont, A.S.; Rosenwasser, R.; Gonzalez, L.F. The case for family screening for intracranial aneurysms. Neurosurg. Focus, 2011, 31(6), E8.
(c) Kang, H.; Peng, T.; Qian, Z.; Li, Y.; Jiang, C.; Ji, W.; Wu, J.; Xu, W.; Wen, X.; Liu, A. Impact of hypertension and smoking on the rupture of intracranial aneurysms and their joint effect. Neurol. Neurochir. Pol., 2015, 49(2), 121-125.
[7]
Jamous, M.A.; Nagahiro, S.; Kitazato, K.T.; Tamura, T.; Kuwayama, K.; Satoh, K. Role of estrogen deficiency in the formation and progression of cerebral aneurysms. Part II: Experimental study of the effects of hormone replacement therapy in rats. J. Neurosurg., 2005, 103(6), 1052-1057.
[8]
Xu, Z.; Li, H.; Song, J.; Han, B.; Wang, Z.; Cao, Y.; Wang, S.; Zhao, J. Meta-analysis of microarray-based expression profiles to identify differentially expressed genes in intracranial aneurysms. World Neurosurg., 2017, 97, 661-668.e7.
[9]
Kleinloog, R.; De, M.N.; Verweij, B.H.; Post, J.A.; Gje, R.; Ruigrok, Y.M. Risk factors for intracranial aneurysm rupture: A systematic review. Neurosurgery, 2017, 82(4), 431-440.
[10]
Yoshimura, Y.; Murakami, Y.; Saitoh, M.; Yokoi, T.; Aoki, T.; Miura, K.; Ueshima, H.; Nozaki, K. Statin use and risk of cerebral aneurysm rupture: a hospital-based case-control study in Japan. J. Stroke Cerebrovasc. Dis., 2014, 23(2), 343-348.
[11]
(a) Flandry, R.E., Jr Inflammatory intracranial aneurysms. J. S. C. Med. Assoc., 1994, 90(1), 11-12.
(b) Tulamo, R.; Frosen, J.; Hernesniemi, J.; Niemela, M. Inflammatory changes in the aneurysm wall: A review. J. Neurointerv. Surg., 2010, 2(2), 120-130.
(b) Tulamo, R.; Frosen, J.; Hernesniemi, J.; Niemela, M. Inflammatory changes in the aneurysm wall: A review. J. Neurointerv. Surg., 2010, 2(2), 120-130.
[12]
(a) Ingebrigtsen, T.; Morgan, M.K.; Faulder, K.; Ingebrigtsen, L.; Sparr, T.; Schirmer, H. Bifurcation geometry and the presence of cerebral artery aneurysms. J. Neurosurg., 2004, 101(1), 108.
(b) Lee, S.W.; Antiga, L.; Spence, J.D.; Steinman, D.A. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke, 2008, 39(8), 2341-2347.
(b) Lee, S.W.; Antiga, L.; Spence, J.D.; Steinman, D.A. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke, 2008, 39(8), 2341-2347.
[13]
Wermer, M.J.; van der Schaaf, I.C.; Algra, A.; Rinkel, G.J. Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: An updated meta-analysis. Stroke, 2007, 38(4), 1404-1410.
[14]
(a) Nixon, A.M.; Gunel, M.; Sumpio, B.E. The critical role of hemodynamics in the development of cerebral vascular disease. J. Neurosurg., 2010, 112(6), 1240.
(b) Alnaes, M.S.; Isaksen, J.; Mardal, K.A.; Romner, B.; Morgan, M.K.; Ingebrigtsen, T. Computation of hemodynamics in the circle of Willis. Stroke, 2007, 38(9), 2500-2505.
(b) Alnaes, M.S.; Isaksen, J.; Mardal, K.A.; Romner, B.; Morgan, M.K.; Ingebrigtsen, T. Computation of hemodynamics in the circle of Willis. Stroke, 2007, 38(9), 2500-2505.
[15]
Prado, C.M.; Ramos, S.G.; Alves-Filho, J.C.; Jr, J.E.; Cunha, F.Q.; Rossi, M.A. PO9-253 wall shear stress and stretch differentially affect aorta remodeling in rats. J. Hypertens., 2006, 24(3), 503-515.
[16]
Dardik, A.; Chen, L.; Frattini, J.; Asada, H.; Aziz, F.; Kudo, F.A.; Sumpio, B.E. Differential effects of orbital and laminar shear stress on endothelial cells. J. Vasc. Surg., 2005, 41(5), 869-880.
[17]
Canham, P.B.; Finlay, H.M. Morphometry of medial gaps of human brain artery branches. Stroke, 2004, 35(5), 1153.
[18]
Wang, Z.; Kolega, J.; Hoi, Y.; Gao, L.; Swartz, D.D.; Levy, E.I.; Mocco, J.; Meng, H. Molecular alterations associated with aneurysmal remodeling are localized in the high hemodynamic stress region of a created carotid bifurcation. Neurosurgery, 2009, 65(1), 169.
[19]
Boussel, L.; Rayz, V.; McCulloch, C.; Martin, A.; Acevedo-Bolton, G.; Lawton, M.; Higashida, R.; Smith, W.S.; Young, W.L.; Saloner, D. Aneurysm growth occurs at region of low wall shear stress: Patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke, 2008, 39(11), 2997-3002.
[20]
Frösen, J.; Piippo, A.; Paetau, A.; Kangasniemi, M.; Niemelä, M.; Hernesniemi, J.; Jääskeläinen, J. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture histological analysis of 24 unruptured and 42 ruptured cases. Stroke, 2004, 35(10), 2287-2293.
[21]
Raghavan, M.L.; Ma, B.; Harbaugh, R.E. Quantified aneurysm shape and rupture risk. J. Neurosurg., 2005, 102(2), 355.
[22]
(a) Humphrey, J.D.; Taylor, C.A. Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Annu. Rev. Biomed. Eng., 2008, 10(10), 221-246.
(b) Hassan, T.; Timofeev, E.V.; Saito, T.; Shimizu, H.; Ezura, M.; Matsumoto, Y.; Takayama, K.; Tominaga, T.; Takahashi, A. A proposed parent vessel geometry-based categorization of saccular intracranial aneurysms: Computational flow dynamics analysis of the risk factors for lesion rupture. J. Neurosurg., 2005, 103(4), 662-680.
(b) Hassan, T.; Timofeev, E.V.; Saito, T.; Shimizu, H.; Ezura, M.; Matsumoto, Y.; Takayama, K.; Tominaga, T.; Takahashi, A. A proposed parent vessel geometry-based categorization of saccular intracranial aneurysms: Computational flow dynamics analysis of the risk factors for lesion rupture. J. Neurosurg., 2005, 103(4), 662-680.
[23]
Morimoto, M.; Miyamoto, S.; Mizoguchi, A.; Kume, N.; Kita, T.; Hashimoto, N. Mouse model of cerebral aneurysm experimental induction by renal hypertension and local hemodynamic changes. Stroke, 2002, 33(7), 1911-1915.
[24]
Moriwaki, T.; Takagi, Y.; Sadamasa, N.; Aoki, T.; Nozaki, K.; Hashimoto, N. Impaired progression of cerebral aneurysms in interleukin-1beta-deficient mice. Stroke, 2006, 37(3), 900-905.
[25]
(a) Aoki, T.; Moriwaki, T.; Takagi, Y.; Kataoka, H.; Yang, J.; Nozaki, K.; Hashimoto, N. The efficacy of apolipoprotein E deficiency in cerebral aneurysm formation. Int. J. Mol. Med., 2008, 21(4), 453-459.
(b) Aoki, T.; Nishimura, M.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Hashimoto, N. Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox(-/-) mice. Lab. Invest., 2009, 89(7), 730-741.
(b) Aoki, T.; Nishimura, M.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Hashimoto, N. Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox(-/-) mice. Lab. Invest., 2009, 89(7), 730-741.
[26]
(a) Chalouhi, N.; Points, L.; Pierce, G.L.; Ballas, Z.; Jabbour, P.; Hasan, D. Localized increase of chemokines in the lumen of human cerebral aneurysms. Stroke, 2013, 44(9), 2594-2597.
(b) Aoki, T.; Koseki, H.; Miyata, H.; Abekura, Y.; Shimizu, K. Intracranial aneurysm as an inflammation-related disease. No Shinkei Geka, 2018, 46(4), 275-294.
(b) Aoki, T.; Koseki, H.; Miyata, H.; Abekura, Y.; Shimizu, K. Intracranial aneurysm as an inflammation-related disease. No Shinkei Geka, 2018, 46(4), 275-294.
[27]
Fennell, V.S.; Kalani, M.Y.; Atwal, G.; Martirosyan, N.L.; Spetzler, R.F. Biology of saccular cerebral aneurysms: A review of current understanding and future directions. Front. Surg., 2016, 3, 43.
[28]
(a) Pawlowska, E.; Szczepanska, J.; Wisniewski, K.; Tokarz, P.; Jaskólski, D.J.; Blasiak, J. NF-κB-mediated inflammation in the pathogenesis of intracranial aneurysm and subarachnoid hemorrhage. Does autophagy play a role? Int. J. Mol. Sci., 2018, 19(4), pii: E1245.
(b) Sawyer, D.M.; Pace, L.A.; Pascale, C.L.; Kutchin, A.C.; O’Neill, B.E.; Starke, R.M.; Dumont, A.S. Lymphocytes influence intracranial aneurysm formation and rupture: role of extracellular matrix remodeling and phenotypic modulation of vascular smooth muscle cells. J. Neuroinflammation, 2016, 13(1), 185.
(c) Aoki, T.; Fukuda, M.; Nishimura, M.; Nozaki, K.; Narumiya, S. Critical role of TNF-alpha-TNFR1 signaling in intracranial aneurysm formation. Acta Neuropathol. Commun., 2014, 2, 34.
(b) Sawyer, D.M.; Pace, L.A.; Pascale, C.L.; Kutchin, A.C.; O’Neill, B.E.; Starke, R.M.; Dumont, A.S. Lymphocytes influence intracranial aneurysm formation and rupture: role of extracellular matrix remodeling and phenotypic modulation of vascular smooth muscle cells. J. Neuroinflammation, 2016, 13(1), 185.
(c) Aoki, T.; Fukuda, M.; Nishimura, M.; Nozaki, K.; Narumiya, S. Critical role of TNF-alpha-TNFR1 signaling in intracranial aneurysm formation. Acta Neuropathol. Commun., 2014, 2, 34.
[29]
Shi, C.; Awad, I.A.; Jafari, N.; Lin, S.; Du, P.; Hage, Z.A.; Shenkar, R.; Getch, C.C.; Bredel, M.; Batjer, H.H.; Bendok, B.R. Genomics of human intracranial aneurysm wall. Stroke, 2009, 40(4), 1252.
[30]
Kleinloog, R.; Verweij, B.H.; van der Vlies, P.; Deelen, P.; Swertz, M.A.; de Muynck, L.; Van Damme, P.; Giuliani, F.; Regli, L.; van der Zwan, A.; Berkelbach van der Sprenkel, J.W.; Han, K.S.; Gosselaar, P.; van Rijen, P.C.; Korkmaz, E.; Post, J.A.; Rinkel, G.J.; Veldink, J.H.; Ruigrok, Y.M. RNA sequencing analysis of intracranial aneurysm walls reveals involvement of lysosomes and immunoglobulins in rupture. Stroke, 2017, 47(5), 1286.
[31]
Pera, J.; Korostynski, M.; Krzyszkowski, T.; Czopek, J.; Slowik, A.; Dziedzic, T.; Piechota, M.; Stachura, K.; Moskala, M.; Przewlocki, R.; Szczudlik, A. Gene expression profiles in human ruptured and unruptured intracranial aneurysms: What is the role of inflammation? Stroke, 2010, 41(2), 224-231.
[32]
Gimbrone, M.A. Jr. Endothelial dysfunction, hemodynamic forces, and atherosclerosis. Ann. N. Y. Acad. Sci., 2010, 902(1), 230-240.
[33]
Metaxa, E.; Meng, H.; Kaluvala, S.R.; Szymanski, M.P.; Paluch, R.A.; Kolega, J. Nitric oxide-dependent stimulation of endothelial cell proliferation by sustained high flow. Am. J. Physiol. Heart Circ. Physiol., 2008, 295(2), H736.
[34]
Jamous, M.A.; Nagahiro, S.; Kitazato, K.T.; Tamura, T.; Aziz, H.A.; Shono, M.; Satoh, K. Endothelial injury and inflammatory response induced by hemodynamic changes preceding intracranial aneurysm formation: Experimental study in rats. J. Neurosurg., 2007, 107(2), 405-411.
[35]
Fan, X.J.; Zhao, H.D.; Yu, G.; Zhong, X.L.; Yao, H.; Yang, Q.D. Role of inflammatory responses in the pathogenesis of human cerebral aneurysm. Genet. Mol. Res., 2015, 14(3), 9062-9070.
[36]
(a) Abruzzo, T.; Kendler, A.; Apkarian, R.; Workman, M.; Khoury, J.C.; Cloft, H.J. Cerebral aneurysm formation in nitric oxide synthase-3 knockout mice. Curr. Neurovasc. Res., 2007, 4(3), 161-169.
(b) Aoki, T.; Kataoka, H.; Shimamura, M.; Nakagami, H.; Wakayama, K.; Moriwaki, T.; Ishibashi, R.; Nozaki, K.; Morishita, R.; Hashimoto, N. NF-kappaB is a key mediator of cerebral aneurysm formation. Circulation, 2007, 116(24), 2830-2840.
(b) Aoki, T.; Kataoka, H.; Shimamura, M.; Nakagami, H.; Wakayama, K.; Moriwaki, T.; Ishibashi, R.; Nozaki, K.; Morishita, R.; Hashimoto, N. NF-kappaB is a key mediator of cerebral aneurysm formation. Circulation, 2007, 116(24), 2830-2840.
[37]
Beckman, J.S.; Koppenol, W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol., 1996, 271(5 Pt 1), C1424-C1437.
[38]
Nathan, C.; Xie, Q.W. Nitric oxide synthases: Roles, tolls, and controls. Cell, 1994, 78(6), 915-918.
[39]
Koide, M.; Kawahara, Y.; Tsuda, T.; Nakayama, I.; Yokoyama, M. Expression of nitric oxide synthase by cytokines in vascular smooth muscle cells. Hypertension, 1994, 23(1)(Suppl.), 45-48.
[40]
Atochin, D.N.; Huang, P.L. Endothelial nitric oxide synthase transgenic models of endothelial dysfunction. Pflugers Arch., 2010, 460(6), 965-974.
[41]
Arnal, J.F.; Dinh-Xuan, A.T.; Pueyo, M.; Darblade, B.; Rami, J. Endothelium-derived nitric oxide and vascular physiology and pathology. Cell. Mol. Life Sci., 1999, 55(8-9), 1078-1087.
[42]
Balligand, J.L.; Feron, O.; Dessy, C. eNOS activation by physical forces: From short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol. Rev., 2009, 89(2), 481.
[43]
Huang, P.L. Unraveling the links between diabetes, obesity, and cardiovascular disease. Circ. Res., 2005, 96(11), 1129-1131.
[44]
Kuhlencordt, P.J.; Gyurko, R.; Han, F.; Scherrer-Crosbie, M.; Aretz, T.H.; Hajjar, R.; Picard, M.H.; Huang, P.L. Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation, 2001, 104(4), 448-454.
[45]
Aoki, T.; Nishimura, M.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Miyamoto, S. Complementary inhibition of cerebral aneurysm formation by eNOS and nNOS. Lab. Invest., 2011, 91(4), 619-626.
[46]
Sadamasa, N.; Nozaki, K.; Hashimoto, N. Disruption of gene for inducible nitric oxide synthase reduces progression of cerebral aneurysms. Stroke, 2003, 34(12), 2980.
[48]
MJ. K.; JA, F. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am. J. Physiol., 1994, 266(1), 628-636.
[49]
Harrison, D.G.; Widder, J.; Grumbach, I.; Chen, W.; Weber, M.; Searles, C. Endothelial mechanotransduction, nitric oxide and vascular inflammation. J. Intern. Med., 2010, 259(4), 351-363.
[51]
Ghosh, S.; Dass, J.F.P. Study of pathway cross-talk interactions with NF-κB leading to its activation via ubiquitination or phosphorylation: A brief review. Gene, 2016, 584(1), 97-109.
[52]
Aoki, T.; Frosen, J.; Fukuda, M.; Bando, K.; Shioi, G.; Tsuji, K.; Ollikainen, E.; Nozaki, K.; Laakkonen, J.; Narumiya, S. Prostaglandin E2-EP2-NF-kappaB signaling in macrophages as a potential therapeutic target for intracranial aneurysms. Sci. Signal., 2017, 10(465), pii: eaah6037.
[53]
Perkins, N.D. Perkins NDThe diverse and complex roles of NF-kappaB subunits in cancer. Nat. Rev. Cancer, 2012, 12(2), 121-132.
[54]
De Meyer, G.R.; Grootaert, M.O.; Michiels, C.F.; Kurdi, A.; Schrijvers, D.M.; Martinet, W. Autophagy in vascular disease. Circ. Res., 2015, 116(3), 468-479.
[55]
Hosaka, K.; Hoh, B.L. Inflammation and cerebral aneurysms. Transl. Stroke Res., 2014, 5(2), 190-198.
[56]
Aoki, T.; Nishimura, M.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Hashimoto, N. Reactive oxygen species modulate growth of cerebral aneurysms: A study using the free radical scavenger edaravone and p47phox(-/-) mice. Lab. Invest., 2009, 89(7), 730-741.
[57]
Kanematsu, Y.; Kanematsu, M.; Kurihara, C.; Tada, Y.; Tsou, T.L.; Rooijen, N.V.; Lawton, M.T.; Young, W.L.; Liang, E.I.; Nuki, Y. Critical roles of macrophages in the formation of intracranial aneurysm. Stroke, 2011, 42(1), 173.
[58]
Bhullar, I.S.; Li, Y.S.; Miao, H.; Zandi, E.; Kim, M.; Shyy, J.Y.; Chien, S. Fluid shear stress activation of IkappaB kinase is integrin-dependent. J. Biol. Chem., 1998, 273(46), 30544-30549.
[59]
Aoki, T.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Egashira, K.; Hashimoto, N. Impact of monocyte chemoattractant protein-1 deficiency on cerebral aneurysm formation. Stroke, 2009, 40(3), 942-951.
[60]
Moore, K.J.; Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell, 2011, 145(3), 341-355.
[61]
Aoki, T.; Kataoka, H.; Morimoto, M.; Nozaki, K.; Hashimoto, N. Macrophage-derived matrix metalloproteinase-2 and -9 promote the progression of cerebral aneurysms in rats. Stroke, 2007, 38(1), 162-169.
[62]
Raffetto, J.D.; Khalil, R.A. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem. Pharmacol., 2008, 75(2), 346-359.
[63]
Hasan, D.; Chalouhi, N.; Jabbour, P.; Hashimoto, T. Macrophage imbalance (M1 vs. M2) and upregulation of mast cells in wall of ruptured human cerebral aneurysms: Preliminary results. J. Neuroinflammation, 2012, 9(1), 222.
[64]
Libby, P.; Tabas, I.; Fredman, G.; Fisher, E.A. Inflammation and its resolution as determinants of acute coronary syndromes. Circ. Res., 2014, 114(12), 1867.
[65]
Nagase, H.; Visse, R.; Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res., 2006, 69(3), 562-573.
[66]
Song, J.; Wu, C.; Zhang, X.; Sorokin, L.M. In vivo processing of CXCL5 (LIX) by matrix metalloproteinase (MMP)-2 and MMP-9 promotes early neutrophil recruitment in IL-1β-induced peritonitis. J. Immunol., 2013, 190(1), 401-410.
[67]
(a) Woo, C.H.; Lim, J.H.; Kim, J.H. Lipopolysaccharide induces matrix metalloproteinase-9 expression via a mitochondrial reactive oxygen species-p38 kinase-activator protein-1 pathway in Raw 264.7 cells. J. Immunol., 2004, 173(11), 6973-6980.
(b) Green, J.A.; Dholakia, S.; Janczar, K.; Ong, C.W.; Moores, R.; Fry, J.; Elkington, P.T.; Roncaroli, F.; Friedland, J.S. Mycobacterium tuberculosis-infected human monocytes down-regulate microglial MMP-2 secretion in CNS tuberculosis via TNFα, NFκB, p38 and caspase 8 dependent pathways. J. Neuroinflammation, 2011, 8(1), 46.
(b) Green, J.A.; Dholakia, S.; Janczar, K.; Ong, C.W.; Moores, R.; Fry, J.; Elkington, P.T.; Roncaroli, F.; Friedland, J.S. Mycobacterium tuberculosis-infected human monocytes down-regulate microglial MMP-2 secretion in CNS tuberculosis via TNFα, NFκB, p38 and caspase 8 dependent pathways. J. Neuroinflammation, 2011, 8(1), 46.
[68]
Chen, Q.; Moulder, K.; Tenkova, T.; Hardy, K.; Olney, J.W.; Romano, C. Excitotoxic cell death dependent on inhibitory receptor activation. Exp. Neurol., 1999, 160(1), 215-225.
[69]
Gurney, K.J.; Estrada, E.Y.; Rosenberg, G.A. Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol. Dis., 2006, 23(1), 87-96.
[70]
Perrotta, I.; Sciangula, A.; Aquila, S.; Mazzulla, S. Matrix metalloproteinase-9 expression in calcified human aortic valves: A histopathologic, immunohistochemical, and ultrastructural study. Appl. Immunohistochem. Mol. Morphol., 2016, 24(2), 128-137.
[71]
Nuki, Y.; Tsou, T.L.; Kurihara, C.; Kanematsu, M.; Kanematsu, Y.; Hashimoto, T. Elastase-induced intracranial aneurysms in hypertensive mice. Hypertension, 2009, 54(6), 1337-1344.
[72]
Xiong, W.; Knispel, R.A.; Dietz, H.C.; Ramirez, F.; Baxter, B.T. Doxycycline delays aneurysm rupture in a mouse model of Marfan syndrome. J. Vasc. Surg., 2008, 47(1), 166-172.
[73]
Aoki, T.; Kataoka, H.; Ishibashi, R.; Nozaki, K.; Hashimoto, N. Simvastatin suppresses the progression of experimentally induced cerebral aneurysms in rats. Stroke, 2008, 39(4), 1276-1285.
[74]
Owens, G.K. Molecular control of vascular smooth muscle cell differentiation and phenotypic plasticity. Novartis Found. Symp., 2007, 283, 174.
[75]
Nakajima, N.; Nagahiro, S.; Sano, T.; Satomi, J.; Satoh, K. Phenotypic modulation of smooth muscle cells in human cerebral aneurysmal walls. Acta Neuropathol., 2000, 100(5), 475-480.
[76]
Chalouhi, N.; Ali, M.S.; Jabbour, P.M.; Tjoumakaris, S.I.; Gonzalez, L.F.; Rosenwasser, R.H.; Koch, W.J.; Dumont, A.S. Biology of intracranial aneurysms: role of inflammation. J. Cereb. Blood Flow Metab., 2012, 32(9), 1659-1676.
[77]
Frösen, J.; Marjamaa, J.; Myllärniemi, M.; Aboramadan, U.; Tulamo, R.; Niemelä, M.; Hernesniemi, J.; Jääskeläinen, J. Contribution of mural and bone marrow-derived neointimal cells to thrombus organization and wall remodeling in a microsurgical murine saccular aneurysm model. Neurosurgery, 2006, 58(5), 936-944.
[78]
Kilic, T.; Sohrabifar, M.; Kurtkaya, O.; Yildirim, O.; Elmaci, I.; Günel, M.; Pamir, M.N. Expression of structural proteins and angiogenic factors in normal arterial and unruptured and ruptured aneurysm walls. Neurosurgery, 2005, 57(5), 997-1007.
[79]
Mérei, F.T.; Gallyas, F. Role of the structural elements of the arterial wall in the formation and growth of intracranial saccular aneurysms. Neurol. Res., 1993, 2(1), 283-303.
[80]
Ali, M.S.; Starke, R.M.; Jabbour, P.M.; Tjoumakaris, S.I.; Gonzalez, L.F.; Rosenwasser, R.H.; Owens, G.K.; Koch, W.J.; Greig, N.H.; Dumont, A.S. TNF-α induces phenotypic modulation in cerebral vascular smooth muscle cells: Implications for cerebral aneurysm pathology. J. Cereb. Blood Flow Metab., 2013, 33(10), 1564-1573.
[81]
Ali, M.S.; Starke, R.M.; Jabbour, P.; Tjoumakaris, S.I.; Gonzalez, L.F.; Rosenwasser, R.H.; Dumont, A.S. 184 infliximab suppresses TNF-[alpha] induced inflammatory phenotype in cerebral vascular smooth muscle cells: Implications for cerebral aneurysm formation. Neurosurgery, 2013, 60, 181.
[82]
Wajant, H.; Pfizenmaier, K.; Scheurich, P. Tumor necrosis factor signaling. Cell Death Differ., 2003, 10(1), 45-65.
[83]
Narayan, N.; Lee, I.H.; Borenstein, R.; Sun, J.; Wong, R.; Tong, G.; Fergusson, M.M.; Liu, J.; Rovira, I.I.; Cheng, H.L. The NAD-dependent deacetylase SIRT2 is required for programmed necrosis. Nature, 2014, 506(7489), 516.
[84]
Maddahi, A.; Kruse, L.S.; Chen, Q.W.; Edvinsson, L. The role of tumor necrosis factor-α and TNF-α receptors in cerebral arteries following cerebral ischemia in rat. J. Neuroinflammation, 2011, 8(1), 1-13.
[85]
Fontanella, M.; Rainero, I.; Gallone, S.; Rubino, E.; Fenoglio, P.; Valfrè, W.; Garbossa, D.; Carlino, C.; Ducati, A.; Pinessi, L. Tumor necrosis factor-alpha gene and cerebral aneurysms. Neurosurgery, 2007, 60(4), 668.
[86]
Jayaraman, T.; Berenstein, V.; Li, X.; Mayer, J.; Silane, M.; Shin, Y.S.; Niimi, Y.; Kilic, T.; Gunel, M.; Berenstein, A. Tumor necrosis factor alpha is a key modulator of inflammation in cerebral aneurysms. Neurosurgery, 2005, 57(3), 558-564.
[87]
(a) Liu, Y.; Li, P.; Hu, X.; Hu, Y.; Sun, H.G.; Ma, W.C.; Qiao, F.; He, M.; You, C. Angiotensin-converting enzyme insertion/deletion gene polymorphism and risk of intracranial aneurysm in a Chinese population. J. Int. Med. Res., 2013, 41(4), 1079-1087.
(b) Cui, H.K.; Yan, R.F.; Ding, X.L.; Zhao, P.; Wu, Q.W.; Wang, H.P.; Qin, H.X.; Tu, J.F.; Yang, R.M. Platelet-derived growth factor-β expression in rabbit models of cerebral vasospasm following subarachnoid hemorrhage. Mol. Med. Rep., 2014, 10(3), 1416.
(c) Ruigrok, Y.M.; Baas, A.F.; Medic, J.; Wijmenga, C.; Rinkel, G.J.E. The transforming growth factor‐β receptor genes and the risk of intracranial aneurysms. Int. J. Stroke, 2012, 7(8), 645-648.
(d) Ollikainen, E.; Tulamo, R.; Lehti, S.; Hernesniemi, J.; Niemelä, M.; Kovanen, P.T.; Frösen, J. Myeloperoxidase associates with degenerative remodeling and rupture of the saccular intracranial aneurysm wall. Eur. J. Clin. Invest., 2018, 77(6), 461-468.
(b) Cui, H.K.; Yan, R.F.; Ding, X.L.; Zhao, P.; Wu, Q.W.; Wang, H.P.; Qin, H.X.; Tu, J.F.; Yang, R.M. Platelet-derived growth factor-β expression in rabbit models of cerebral vasospasm following subarachnoid hemorrhage. Mol. Med. Rep., 2014, 10(3), 1416.
(c) Ruigrok, Y.M.; Baas, A.F.; Medic, J.; Wijmenga, C.; Rinkel, G.J.E. The transforming growth factor‐β receptor genes and the risk of intracranial aneurysms. Int. J. Stroke, 2012, 7(8), 645-648.
(d) Ollikainen, E.; Tulamo, R.; Lehti, S.; Hernesniemi, J.; Niemelä, M.; Kovanen, P.T.; Frösen, J. Myeloperoxidase associates with degenerative remodeling and rupture of the saccular intracranial aneurysm wall. Eur. J. Clin. Invest., 2018, 77(6), 461-468.
[88]
Wang, Y.; Emeto, T.I.; Lee, J.; Marshman, L.; Moran, C.; Seto, S.W.; Golledge, J. Mouse models of intracranial aneurysm. Brain Pathol., 2015, 25(3), 237-247.
[89]
Nasri, A.; Mansour, M.; Brahem, Z.; Kacem, A.; Hassan, A.A.; Derbali, H.; Messelmani, M.; Zaouali, J.; Mrissa, R. Stroke disclosing primary aldosteronism: Report on three cases and review of the literature. Annales Dendocrinologie, 2017, 78(1), 9-13.
[90]
Cun, Y.P.; Xiong, C.J.; Diao, B.; Yang, Y.; Pan, L.; Ma, L.T. Association between angiotensin-converting enzyme insertion/deletion polymorphisms and intracranial aneurysm susceptibility: A meta-analysis. Biomed. Rep., 2017, 6(6), 663-670.
[91]
Pannu, H.; Kim, D.H.; Seaman, C.R.; Van, G.G.; Shete, S.; Milewicz, D.M. Lack of an association between the angiotensin-converting enzyme insertion/deletion polymorphism and intracranial aneurysms in a Caucasian population in the United States. J. Neurosurg., 2005, 103(1), 92.
[92]
Kao, H.W.; Lee, K.W.; Kuo, C.L.; Huang, C.S.; Tseng, W.M.; Liu, C.S.; Lin, C.P. Interleukin-6 as a Prognostic biomarker in ruptured intracranial aneurysms. PLoS One, 2015, 10(7), e0132115.
[93]
Zheng, S.; Su, A.; Sun, H.; You, C. The association between interleukin-6 gene polymorphisms and intracranial aneurysms: A meta-analysis. Hum. Immunol., 2013, 74(12), 1679-1683.
[94]
Liu, B.; Zhang, J.N.; Pu, P.Y. Expressions of PDGF-B and collagen type III in the remodeling of experimental saccular aneurysm in rats. Neurol. Res., 2008, 30(6), 632-638.
[95]
Sathyan, S.; Koshy, L.V.; Srinivas, L.; Easwer, H.V.; Premkumar, S.; Nair, S.; Bhattacharya, R.N.; Alapatt, J.P.; Banerjee, M. Erratum to: Pathogenesis of intracranial aneurysm is mediated by proinflammatory cytokine TNFA and IFNG and through stochastic regulation of IL10 and TGFB1 by comorbid factors. J. Neuroinflammation, 2015, 12(1), 135.
[96]
Kosierkiewicz, T.A.; Factor, S.M.; Dickson, D.W. Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J. Neuropathol. Exp. Neurol., 1994, 53(4), 399-406.
[97]
Chyatte, D.; Bruno, G.; Desai, S.; Todor, D.R. Inflammation and intracranial aneurysms. Neurosurgery, 1999, 45(5), 1137.
[98]
Lintermans, L.L.; Stegeman, C.A.; Heeringa, P.; Abdulahad, W.H. T cells in vascular inflammatory diseases. Front. Immunol., 2014, 5, 504.
[99]
Frösen, J.; Tulamo, R.; Heikura, T.; Sammalkorpi, S.; Niemelä, M.; Hernesniemi, J.; Levonen, A.; Hörkkö, S. YläHerttuala, S. Lipid accumulation, lipid oxidation, and low plasma levels of acquired antibodies against oxidized lipids associate with degeneration and rupture of the intracranial aneurysm wall. Acta Neuropathol. Commun., 2013, 1(1), 71.
[100]
Yu, Z.; Jiang, Y.; Yong, P.; Zhang, M. The quantitative and functional changes of postoperative peripheral blood immune cell subsets relate to prognosis of patients with subarachnoid hemorrhage: A preliminary study. World Neurosurg., 2017, 108, 206-215.
[101]
Aoki, T.; Nishimura, M. The development and the use of experimental animal models to study the underlying mechanisms of CA formation. J. Biomed. Biotechnol., 2011, 2011, 257-260.
[102]
(a) Tulamo, R.; Frosen, J.; Junnikkala, S.; Paetau, A.; Pitkaniemi, J.; Kangasniemi, M.; Niemela, M.; Jaaskelainen, J.; Jokitalo, E.; Karatas, A.; Hernesniemi, J.; Meri, S. Complement activation associates with saccular cerebral artery aneurysm wall degeneration and rupture. Neurosurgery, 2006, 59(5), 1069-1076 discussion 1076-1077;-.
(b) Tulamo, R.; Frösen, J.; Junnikkala, S.; Paetau, A.; Kangasniemi, M.; Peláez, J.; Hernesniemi, J.; Niemelä, M.; Meri, S. Complement system becomes activated by the classical pathway in intracranial aneurysm walls. Lab. Invest., 2010, 90(2), 168.
(b) Tulamo, R.; Frösen, J.; Junnikkala, S.; Paetau, A.; Kangasniemi, M.; Peláez, J.; Hernesniemi, J.; Niemelä, M.; Meri, S. Complement system becomes activated by the classical pathway in intracranial aneurysm walls. Lab. Invest., 2010, 90(2), 168.
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