Genetic and cellular evidence of vascular inflammation in neurofibromin-deficient mice and humans

Journal of Clinical Investigation

Volumn 120, Issue 3, 2010, Pages 859-870

  Lasater, Elisabeth A ^a   Li, Fang ^a   Bessler, Waylan K ^a   Estes, Myka L ^a   Vemula, Sasidhar ^a   Hingtgen, Cynthia M ^a   Dinauer, Mary C ^a   Kapur, Reuben ^a   Conway, Simon J ^a   Ingram Jr , David A ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRACTALKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUROFIBROMIN; TUMOR NECROSIS FACTOR ALPHA;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BLOOD VESSEL INJURY; BLOOD VESSEL WALL; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C57BL 6 MOUSE; CAROTID ARTERY LIGATION; CELL LINEAGE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOLOGY; ENDOTHELIUM CELL; GENE INACTIVATION; GENETICS; GENOTYPE; HETEROZYGOTE; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; INTIMA; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; VASCULITIS;

ADOLESCENT; ADULT; ANIMALS; BONE MARROW CELLS; ENDOTHELIAL CELLS; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; VASCULITIS;

EID: 77949660093     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI41443     Document Type: Article

References (67)

1. Riccardi VM. Neurofibromatosis: past, present, and future. N Engl J Med. 1991;324(18):1283-1285.
2. Viskochil D, et al. Deletions and a translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell. 1990;62(1):187-192.
3. Rasmussen SA, Friedman JM. NF1 gene and neurofibromatosis 1. Am J Epidemiol. 2000;151(1):33-40.
4. Ward BA, Gutmann DH. Neurofibromatosis 1: from lab bench to clinic. Pediatr Neurol. 2005; 32(4):221-228.
5. Friedman JM, et al. Cardiovascular disease in neurofibromatosis 1: report of the NF1 Cardiovascular Task Force. Genet Med. 2002;4(3):105-111.
6. Rasmussen SA, Yang Q, Friedman JM. Mortality in neurofibromatosis 1: an analysis using U.S. death certificates. Am J Hum Genet. 2001;68(5):1110-1118.
7. Rosser TL, Vezina G, Packer RJ. Cerebrovascular abnormalities in a population of children with neurofibromatosis type 1. Neurology. 2005;64(3):553-555.
8. Hamilton SJ, Friedman JM. Insights into the pathogenesis of neurofibromatosis 1 vasculopathy. Clin Genet. 2000;58(5):341-344.
9. Xu J, Ismat FA, Wang T, Yang J, Epstein JA. NF1 regulates a Ras-dependent vascular smooth muscle proliferative injury response. Circulation. 2007; 116(19):2148-2156.
10. Lasater EA, et al. Nf1+/- mice have increased neointima formation via hyperactivation of a Gleevec sensitive molecular pathway. Hum Mol Genet. 2008; 17(15):2336-2344.
11. Kofler S, Nickel T, Weis M. Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. Clin Sci (Lond). 2005;108:205-213.
12. Szmitko PE, et al. New markers of inflammation and endothelial cell activation: part I. Circulation. 2003; 108(16):1917-1923.
13. Ingram DA, et al. Hyperactivation of p21ras and the hematopoietic- specific Rho GTPase, Rac2, cooperate to alter the proliferation of neurofibromin deficient mast cells in vivo and in vitro. J Exp Med. 2001;194(1):57-70.
14. Ingram DA, et al. Genetic and biochemical evidence that haploinsufficiency of the Nf1 tumor suppressor gene modulates melanocyte and mast cell fates in vivo. J Exp Med. 2000;191(1):181-188.
15. Li F, et al. Neurofibromin is a novel regulator of RASinduced signals in primary vascular smooth muscle cells. Hum Mol Genet. 2006;15(11):1921- 1930.
16. Munchhof AM, et al. Neurofibroma-associated growth factors activate a distinct signaling network to alter the function of neurofibromindeficient endothelial cells. Hum Mol Genet. 2006; 15(11):1858-1869.
17. Kisanuki YY, et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230(2):230-242.
18. Holtwick R, et al. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci U S A. 2002;99(10):7142-7147.
19. Gitler AD, et al. Nf1 has an essential role in endothelial cells. Nat Genet. 2003;33(1):75-79.
20. Iwama A, et al. Molecular cloning and characterization of mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem Biophys Res Commun. 1993; 195(1):301-309.
21. Schlaeger TM, et al. Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc Natl Acad Sci U S A. 1997; 94(7):3058-3063.
22. Kumar A, Lindner V. Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol. 1997; 17(10):2238-2244.
23. Kuhel DG, Zhu B, Witte DP, Hui DY. Distinction in genetic determinants for injury-induced neointimal hyperplasia and diet-induced atherosclerosis in inbred mice. Arterioscler Thromb Vasc Biol. 2002;22(6):955-960.
24. Simon DI, Dhen Z, Seifert P, Edelman ER, Ballantyne CM, Rogers C. Decreased neointimal formation in Mac-1(-/-) mice reveals a role for inflammation in vascular repair after angioplasty. J Clin Invest. 2000;105(3):293-300.
25. Chamberlain J, et al. Interleukin-1beta and signaling of interleukin-1 in vascular wall and circulating cells modulates the extent of neointima formation in mice. Am J Pathol. 2006;168(4):1396-1403.
26. Libby P, Shi GP. Mast cells as mediators and modulators of atherogenesis. Circulation. 2007; 115(19):2471-2473.
27. Murayama H, et al. Deficiency of tumour necrosis factor-alpha and interferon-gamma in bone marrow cells synergistically inhibits neointimal formation following vascular injury. Cardiovasc Res. 2008;80(2):175-180.
28. Ingram DA, et al. Lymphoproliferative defects in mice lacking the expression of neurofibromin: functional and biochemical consequences of Nf1 deficiency in T-cell development and function. Blood. 2002;100(10):3656-3662.
29. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135-1143.
30. Schlitt A, et al. CD14+CD16+ monocytes in coronary artery disease and their relationship to serum TNFalpha levels. Thromb Haemost. 2004;92(2):419-424.
31. Umehara H, Bloom ET, Okazaki T, Nagano Y, Yoshie O, Imai T. Fractalkine in vascular biology: from basic research to clinical disease. Arterioscler Thromb Vasc Biol. 2004;24(1):34-40.
32. Todd RF 3rd, Van Agthoven A, Schlossman SF, Terhorst C. Structural analysis of differentiation antigens Mo1 and Mo2 on human monocytes. Hybridoma. 1982;1(3):329-337.
33. Grage-Griebenow E, Flad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukoc Biol. 2001;69(1):11-20.
34. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005; 352(16):1685-1695.
35. Abel PM, et al. Heterogeneity of peripheral blood monocyte populations in human immunodeficiency virus-1 seropositive patients. FEMS Microbiol Immunol. 1992;5(5-6):317-323.
36. Cesari M, et al. Inflammatory markers and onset of cardiovascular events: results from the Health ABC study. Circulation. 2003;108(19):2317-2322.
37. Lindmark E, Diderholm E, Wallentin L, Siegbahn A. Relationship between interleukin 6 and mortality in patients with unstable coronary artery disease: effects of an early invasive or noninvasive strategy. JAMA. 2001;286(17):2107-2113.
38. Luc G, et al. C-reactive protein, interleukin-6, and fibrinogen as predictors of coronary heart disease: the PRIME Study. Arterioscler Thromb Vasc Biol. 2003; 23(7):1255-1261.
39. Davies MJ, et al. The expression of the adhesion molecules ICAM-1, VCAM-1, PECAM, and Eselectin in human atherosclerosis. J Pathol. 1993; 171(3):223-229.
40. Fong AM, et al. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J Exp Med. 1998;188(8):1413-1419.
41. Goda S, et al. CX3C-chemokine, fractalkineenhanced adhesion of THP-1 cells to endothelial cells through integrin-dependent and -independent mechanisms. J Immunol. 2000;164(8):4313-4320.
42. Wang CH, et al. Stem cell factor deficiency is vasculoprotective: unraveling a new therapeutic potential of imatinib mesylate. Circ Res. 2006;99(6):617-625.
43. Mombouli JV, Vanhoutte PM. Endothelial dysfunction: from physiology to therapy. J Mol Cell Cardiol. 1999;31(1):61-74.
44. Rubanyi GM. The role of endothelium in cardiovascular homeostasis and diseases. J Cardiovasc Pharmacol. 1993;22(suppl 4):S1-S14.
45. Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ Res. 1998;82(5):532-539.
46. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230-239; discussion 239-240.
47. Rao RM, Yang L, Garcia-Cardena G, Luscinskas FW. Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ Res. 2007;101(3):234-247.
48. Danenberg HD, et al. Systemic inflammation induced by lipopolysaccharide increases neointimal formation after balloon and stent injury in rabbits. Circulation 2002;105(24):2917-2922.
49. Shiba Y, et al. M-CSF accelerates neointimal formation in the early phase after vascular injury in mice: the critical role of the SDF-1-CXCR4 system. Arterioscler Thromb Vasc Biol. 2007;27(2):283-289.
50. Ikeda U, Shimada K. Matrix metalloproteinases and coronary artery diseases. Clin Cardiol. 2003; 26(2):55-59.
51. Cho A, Reidy MA. Matrix metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ Res. 2002;91(9):845-851.
52. Kuzuya M, et al. Deficiency of gelatinase a suppresses smooth muscle cell invasion and development of experimental intimal hyperplasia. Circulation. 2003;108(11):1375-1381.
53. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest. 1983;49(3):327-333.
54. Daginakatte GC, Gutmann DH. Neurofibromatosis-1 (Nf1) heterozygous brain microglia elaborate paracrine factors that promote Nf1-deficient astrocyte and glioma growth. Hum Mol Genet. 2007; 16(9):1098-1112.
55. +/-- and c-kitdependent bone marrow. Cell. 2008;135(3):437-448.
56. Sironi M, et al. IL-1 stimulates IL-6 production in endothelial cells. J Immunol. 1989;142(2):549-553.
57. Iversen PO, Nicolaysen A, Kvernebo K, Benestad HB, Nicolaysen G. Human cytokines modulate arterial vascular tone via endothelial receptors. Pflugers Arch. 1999;439(1-2):93-100.
58. Bazan JF, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature. 1997; 385(6617):640-644.
59. Imai T, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell. 1997;91(4):521-530.
60. Ancuta P, et al. Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med. 2003;197(12):1701-1707.
61. Liu P, Patil S, Rojas M, Fong AM, Smyth SS, Patel DD. CX3CR1 deficiency confers protection from intimal hyperplasia after arterial injury. Arterioscler Thromb Vasc Biol. 2006;26(9):2056-2062.
62. Zhang YY, et al. Nf1 regulates hematopoietic progenitor cell growth and ras signaling in response to multiple cytokines. J Exp Med. 1998;187(11):1893-1902.
63. Zhu Y, et al. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev. 2001; 15(7):859-876.
64. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 1997;407(3):313-319.
65. Munugalavadla V, Borneo J, Ingram DA, Kapur R. p85alpha subunit of class IA PI-3 kinase is crucial for macrophage growth and migration. Blood. 2005;106(1):103-109.
66. [No authors listed]. Neurofibromatosis. Conference statement. National Institutes of Health Consensus Development Conference. Arch Neurol. 1988;45(5):575-578.
67. Yoder MC, et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood. 2007; 109(5):1801-1809.