Role of circulating karyocytes in the initiation and progression of atherosclerosis

Hypertension

Volumn 47, Issue 5, 2006, Pages 803-810

  Chon, Helena ^a   Verhaar, Marianne C ^a   Koomans, Hein A ^a   Joles, Jaap A ^a   Braam, Branko ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Atherosclerosis; Gene expression; Leukocytes; Oxidative stress

Indexed keywords

ANGIOTENSIN II; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL WALL; BONE MARROW CELL; CARDIOVASCULAR RISK; CELL FUNCTION; CELL PROLIFERATION; DIAGNOSTIC ACCURACY; DIAGNOSTIC PROCEDURE; DIAGNOSTIC VALUE; DISEASE ASSOCIATION; ESSENTIAL HYPERTENSION; FOAM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; KARYOCYTE; LEUKOCYTE FUNCTION; MONOCYTE; NONHUMAN; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROGNOSIS; RISK ASSESSMENT; RISK FACTOR; SHORT SURVEY; STEM CELL; TRANSCRIPTION INITIATION; TREATMENT PLANNING; BIOLOGICAL MODEL; BLOOD CELL; DISEASE COURSE; REVIEW;

ATHEROSCLEROSIS; BLOOD CELLS; DISEASE PROGRESSION; HUMANS; MODELS, CARDIOVASCULAR;

EID: 33646122445     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.HYP.0000210554.61293.90     Document Type: Short Survey

References (91)

1. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, Badimon JJ, Stefanadis C, Moreno P, Pasterkamp G, Fayad Z, Stone PH, Waxman S, Raggi P, Madjid M, Zarrabi A, Burke A, Yuan C, Fitzgerald PJ, Siscovick DS, de Korte CL, Aikawa M, Airaksinen KE, Assmann G, Becker CR, Chesebro JH, Farb A, Galis ZS, Jackson C, Jang IK, Koenig W, Lodder RA, March K, Demirovic J, Navab M, Priori SG, Rekhter MD, Bahr R, Grundy SM, Mehran R, Colombo A, Boerwinkle E, Ballantyne C, Insull W Jr, Schwartz RS, Vogel R, Serruys PW, Hansson GK, Faxon DP, Kaul S, Drexler H, Greenland P, Muller JE, Virmani R, Ridker PM, Zipes DP, Shah PK, Willerson JT. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. Circulation. 2003;108:1772-1778.
2. Collins RG, Velji R, Guevara NV, Hicks MJ, Chan L, Beaudet AL. P-Selectin or intercellular adhesion molecule (ICAM)-1 deficiency substantially protects against atherosclerosis in apolipoprotein E-deficient mice. J Exp Med. 2000;191:189-194.
3. Nageh MF, Sandberg ET, Marotti KR, Lin AH, Melchior EP, Bullard DC, Beaudet AL. Deficiency of inflammatory cell adhesion molecules protects against atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 1997;17:1517-1520.
4. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
5. Dorffel Y, Franz S, Pruss A, Neumann G, Rohde W, Burmester GR, Scholze J. Preactivated monocytes from hypertensive patients as a factor for atherosclerosis? Atherosclerosis. 2001;157:151-160.
6. Hong YH, Peng HB, La Fata V, Liao JK. Hydrogen peroxide-mediated transcriptional induction of macrophage colony-stimulating factor by TGF-β1. J Immunol. 1997;159:2418-2423.
7. Chen YH, Yet SF, Perrella MA. Role of heme oxygenase-1 in the regulation of blood pressure and cardiac function. Exp Biol Med (Maywood). 2003;228:447-453.
8. Osterud B, Bjorklid E. Role of monocytes in atherogenesis. Physiol Rev. 2003;83:1069-1112.
9. Choi J, Enis DR, Koh KP, Shiao SL, Pober JS. T lymphocyte-endothelial cell interactions. Annu Rev Immunol. 2004;22:683-709.
10. Grimm M, Spiecker M, De Caterina R, Shin WS, Liao JK. Inhibition of major histocompatibility complex class II gene transcription by nitric oxide and antioxidants. J Biol Chem. 2002;277:26460-26467.
11. Diaz MN, Frei B, Vita JA, Keaney JF Jr. Antioxidants and atherosclerotic heart disease. N Engl J Med. 1997;337:408-416.
12. Waltner-Romen M, Falkensammer G, Rabl W, Wick G. A previously unrecognized site of local accumulation of mononuclear cells. The vascular-associated lymphoid tissue. J Histochem Cytochem. 1998;46:1347-1350.
13. Laurat E, Poirier B, Tupin E, Caligiuri G, Hansson GK, Bariety J, Nicoletti A. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E-knockout mice. Circulation. 2001;104:197-202.
14. Tupin E, Nicoletti A, Elhage R, Rudling M, Ljunggren HG, Hansson GK, Berne GP. CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med. 2004;199:417-422.
15. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
16. Parenti A, Bellik L, Brogelli L, Filippi S, Ledda F. Endogenous VEGF-A is responsible for mitogenic effects of MCP-1 on vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2004;286:H1978-H1984.
17. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-126.
18. Haque NS, Fallon JT, Pan JJ, Taubman MB, Harpel PC. Chemokine receptor-8 (CCR8) mediates human vascular smooth muscle cell chemotaxis and metalloproteinase-2 secretion. Blood. 2004;103:1296-1304.
19. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
20. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
21. Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K, Folkman J. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A. 2003;100:4736-4741.
22. Corazzi T, Leone M, Roberti R, Del Soldato P, Gresele P. Effect of nitric oxide-donating agents on human monocyte cyclooxygenase-2. Biochem Biophys Res Commun. 2003;311:897-903.
23. Braam B, de Roos R, Dijk A, Boer P, Post JA, Kemmeren PP, Holstege FC, Bluysen HA, Koomans HA. Nitric oxide donor induces temporal and dose-dependent reduction of gene expression in human endothelial cells. Am J Physiol Heart Circ Physiol. 2004;287:H1977-H1986.
24. Rabelink TJ, Koomans HA. Endothelial function and the kidney. An emerging target for cardiovascular therapy. Drugs. 1997;53(suppl 1):11-19.
25. Eisenthal A, Gelfand A, Misonzhnik F, Trejo L, Schwartz I, Skornick Y, Lifschitz-Mercer B. Exposure of human peripheral blood mononuclear cells (PBMC) to hydrostatic pressure increases their proliferative response to phytohemagglutinin A (PHA) and anti-CD3 antibody. Immunol Invest. 1999;28:55-65.
26. Achard JM, Bubien JK, Benos DJ, Warnock DG. Stretch modulates amiloride sensitivity and cation selectivity of sodium channels in human B lymphocytes. Am J Physiol. 1996;270:C224-C234.
27. Sakamoto H, Aikawa M, Hill CC, Weiss D, Taylor WR, Libby P, Lee RT. Biomechanical strain induces class a scavenger receptor expression in human monocyte/macrophages and THP-1 cells: a potential mechanism of increased atherosclerosis in hypertension. Circulation. 2001;104:109-114.
28. Ashida N, Takechi H, Kita T, Arai H. Vortex-mediated mechanical stress induces integrin-dependent cell adhesion mediated by inositol 1,4,5-trisphosphate-sensitive Ca2+ release in THP-1 cells. J Biol Chem. 2003;278:9327-9331.
29. Yang JH, Sakamoto H, Xu EC, Lee RT. Biomechanical regulation of human monocyte/macrophage molecular function. Am J Pathol. 2000;156:1797-1804.
30. Fukuda N, Nakayama M, Jian T, Satoh C, Nakayama T, Soma M, Izumi Y, Kanmatsuse K. Leukocyte angiotensin II levels inpatients with essential hypertension:relation to insulin resistance. Am J Hypertens. 2003;16:129-134.
31. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003;42:1075-1081.
32. Song K, Shiota N, Takai S, Takashima H, Iwasaki H, Kim S, Miyazaki M. Induction of angiotensin converting enzyme and angiotensin II receptors in the atherosclerotic aorta of high-cholesterol fed Cynomolgus monkeys. Atherosclerosis. 1998;138:171-182.
33. Schieffer B, Schieffer E, Hilfiker-Kleiner D, Hilfiker A, Kovanen PT, Kaartinen M, Nussberger J, Harringer W, Drexler H. Expression of angiotensin II and interleukin 6 in human coronary atherosclerotic plaques: potential implications for inflammation and plaque instability. Circulation. 2000;101:1372-1378.
34. Chon H, Gaillard CA, van der Meijden BB, Dijstelbloem HM, Kraaijenhagen RJ, van Leenen D, Holstege FC, Joles JA, Bluyssen HA, Koomans HA, Braam B. Broadly altered gene expression in blood leukocytes in essential hypertension is absent during treatment. Hypertension. 2004;43:947-951.
35. Sela S, Mazor R, Amsalam M, Yagil C, Yagil Y, Kristal B. Primed polymorphonuclear leukocytes, oxidative stress, and inflammation antecede hypertension in the Sabra rat. Hypertension. 2004;44:764-769.
36. Kintscher U, Wakino S, Kim S, Fleck E, Hsueh WA, Law RE. Angiotensin II induces migration and Pyk2/paxillin phosphorylation of human monocytes. Hypertension. 2001;37:587-593.
37. Nahmod KA, Vermeulen ME, Raiden S, Salamone G, Gamberale R, Fernandez-Calotti P, Alvarez A, Nahmod V, Giordano M, Geffner JR. Control of dendritic cell differentiation by angiotensin II. Faseb J. 2003;17:491-493.
38. Abdalla S, Lother H, Langer A, El Faramawy Y, Quitterer U. Factor XIIIA transglutaminase crosslinks AT(1) receptor dimers of monocytes at the onset of atherosclerosis. Cell. 2004;119:343-354.
39. Nobuhiko A, Suganuma E, Babaev VR, Fogo A, Swift LL, Linton MF, Fazio S, Ichikawa I, Kon V. Angiotensin II amplifies macrophage-driven atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2143-2148.
40. Kristal B, Shurtz-Swirski R, Chezar J, Manaster J, Levy R, Shapiro G, Weissman I, Shasha SM, Sela S. Participation of peripheral polymorphonuclear leukocytes in the oxidative stress and inflammation in patients with essential hypertension. Am J Hypertens. 1998;11:921-928.
41. Lassegue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol. 2003;285:R277-R297.
42. Wang H, Nawata J, Kakudo N, Sugimura K, Suzuki J, Sakuma M, Ikeda J, Shirato K. The upregulation of ICAM-1 and P-selectin requires high blood pressure but not circulating renin-angiotensin system in vivo. J Hypertens. 2004;22:1323-1332.
43. Alderman CJ, Bunyard PR, Chain BM, Foreman JC, Leake DS, Katz DR. Effects of oxidised low density lipoprotein on dendritic cells: a possible immunoregulatory component of the atherogenic micro-environment? Cardiovasc Res. 2002;55:806-819.
44. Yagisawa M, Yuo A, Kitagawa S, Yazaki Y, Togawa A, Takaku F. Stimulation and priming of human neutrophils by IL-1 α and IL-1 β: complete inhibition by IL-1 receptor antagonist and no interaction with other cytokines. Exp Hematol. 1995;23:603-608.
45. Kamimura D, Ishihara K, Hirano T. IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol. 2003;149:1-38.
46. Juvonen J, Surcel HM, Satta J, Teppo AM, Bloigu A, Syrjala H, Airaksinen J, Leinonen M, Saikku P, Juvonen T. Elevated circulating levels of inflammatory cytokines in patients with abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol. 1997;17:2843-2847.
47. Saadeddin SM, Habbab MA, Ferns GA. Markers of inflammation and coronary artery disease. Med Sci Monit. 2002;8:RA5-R12.
48. Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:1876-1890.
49. Gupta S, Pablo AM, Jiang X, Wang N, Tall AR, Schindler C. IFN-γ potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99:2752-2761.
50. Whitman SC, Ravisankar P, Elam H, Daugherty A. Exogenous interferon-γ enhances atherosclerosis in apolipoprotein E-/- mice. Am J Pathol. 2000;157:1819-1824.
51. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
52. Rookmaaker MB, Smits AM, Tolboom H, Van 't Wout K, Martens AC, Goldschmeding R, Joles JA, Van Zonneveld AJ, Grone HJ, Rabelink TJ, Verhaar MC. Bone-marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am J Pathol. 2003;163:553-562.
53. Op den Buijs J, Musters M, Verrips T, Post JA, Braam B, van Riel N. Mathematical modeling of vascular endothelial layer maintenance: the role of endothelial cell division, progenitor cell homing, and telomere shortening. Am J Physiol Heart Circ Physiol. 2004;287:H2651-H2658.
54. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Nat Med. 2001;7:738-741.
55. Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood. 2004;104:2761-2766.
56. Hristov M, Erl W, Weber PC. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol. 2003;23:1185-1189.
57. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864.
58. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786.
59. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld AJ. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes. 2004;53:195-199.
60. de Groot K, Bahlmann FH, Sowa J, Koenig J, Menne J, Haller H, Fliser D. Uremia causes endothelial progenitor cell deficiency. Kidney Int. 2004;66:641-646.
61. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593-600.
62. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353:999-1007.
63. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and α-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest. 2001;107:1411-1422.
64. Simper D, Wang S, Deb A, Holmes D, McGregor C, Frantz R, Kushwaha SS, Caplice NM. Endothelial progenitor cells are decreased in blood of cardiac allograft patients with vasculopathy and endothelial cells of non-cardiac origin are enriched in transplant atherosclerosis. Circulation. 2003;108:143-149.
65. Dimmeler S, Zeiher AM. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis? J Mol Med. 2004;82:671-677.
66. George J, Goldstein E, Abashidze S, Deutsch V, Shmilovich H, Finkelstein A, Herz I, Miller H, Keren G. Circulating endothelial progenitor cells in patients with unstable angina: association with systemic inflammation. Eur Heart J. 2004;25:1003-1008.
67. Krankel N, Adams V, Linke A, Gielen S, Erbs S, Lenk K, Schuler G, Hambrecht R. Hyperglycemia reduces survival and impairs function of circulating blood-derived progenitor cells. Arterioscler Thromb Vasc Biol. 2005;25:698-703.
68. Rodgers KE, Xiong S, Steer R, diZerega GS. Effect of angiotensin II on hematopoietic progenitor cell proliferation. Stem Cells. 2000;18:287-294.
69. Imanishi T, Hano T, Nishio I. Angiotensin II potentiates vascular endothelial growth factor-induced proliferation and network formation of endothelial progenitor cells. Hypertens Res. 2004;27:101-108.
70. Min TQ, Zhu CJ, Xiang WX, Hui ZJ, Peng SY. Improvement in endothelial progenitor cells from peripheral blood by ramipril therapy in patients with stable coronary artery disease. Cardiovasc Drugs Ther. 2004;18:203-209.
71. Bahlmann FH, de Groot K, Mueller O, Hertel B, Haller H, Fliser D. Stimulation of endothelial progenitor cells: a new putative therapeutic effect of angiotensin II receptor antagonists. Hypertension. 2005;45:526-529.
72. Imanishi T, Hano T, Nishio I. Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens. 2005;23:97-104.
73. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
74. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415:530-536.
75. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, Coller H, Loh ML, Downing JR, Caligiuri MA, Bloomfield CD, Lander ES. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286:531-537.
76. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J Jr, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, Warnke R, Staudt LM. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503-511.
77. Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, Hurt EM, Zhao H, Averett L, Yang L, Wilson WH, Jaffe ES, Simon R, Klausner RD, Powell J, Duffey PL, Longo DL, Greiner TC, Weisenburger DD, Sanger WG, Dave BJ, Lynch JC, Vose J, Armitage JO, Montserrat E, Lopez-Guillermo A, Grogan TM, Miller TP, LeBlanc M, Ott G, Kvaloy S, Delabie J, Holte H, Krajci P, Stokke T, Staudt LM. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med. 2002;346:1937-1947.
78. Pravenec M, Wallace C, Aitman TJ, Kurtz TW. Gene expression profiling in hypertension research: a critical perspective. Hypertension. 2003;41:3-8.
79. Brazma A, Vilo J. Gene expression data analysis. Microbes Infect. 2001;3:823-829.
80. Rus V, Chen H, Zernetkina V, Magder LS, Mathai S, Hochberg MC, Via CS. Gene expression profiling in peripheral blood mononuclear cells from lupus patients with active and inactive disease. Clin Immunol. 2004;112:231-234.
81. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197:711-723.
82. Bomprezzi R, Ringner M, Kim S, Bittner ML, Khan J, Chen Y, Elkahloun A, Yu A, Bielekova B, Meltzer PS, Martin R, McFarland HF, Trent JM. Gene expression profile in multiple sclerosis patients and healthy controls: identifying pathways relevant to disease. Hum Mol Genet. 2003;12:2191-2199.
83. Olsen N, Sokka T, Seehorn CL, Kraft B, Maas K, Moore J, Aune TM. A gene expression signature for recent onset rheumatoid arthritis in peripheral blood mononuclear cells. Ann Rheum Dis. 2004;63:1387-1392.
84. Jarvis JN, Dozmorov I, Jiang K, Frank MB, Szodoray P, Alex P, Centola M. Novel approaches to gene expression analysis of active polyarticular juvenile rheumatoid arthritis. Arthritis Res Ther. 2004;6:R15-R32.
85. Achiron A, Gurevich M, Magalashvili D, Kishner I, Dolev M, Mandel M. Understanding autoimmune mechanisms in multiple sclerosis using gene expression microarrays: treatment effect and cytokine-related pathways. Clin Dev Immunol. 2004;11:299-305.
86. Flechner SM, Kurian SM, Head SR, Sharp SM, Whisenant TC, Zhang J, Chismar JD, Horvath S, Mondala T, Gilmartin T, Cook DJ, Kay SA, Walker JR, Salomon DR. Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant. 2004;4:1475-1489.
87. Preston GA, Waga I, Alcorta DA, Sasai H, Munger WE, Sullivan P, Phillips B, Jennette JC, Falk RJ. Gene expression profiles of circulating leukocytes correlate with renal disease activity in IgA nephropathy. Kidney Int. 2004;65:420-430.
88. Jison ML, Munson PJ, Barb JJ, Suffredini AF, Talwar S, Logun C, Raghavachari N, Beigel JH, Shelhamer JH, Danner RL, Gladwin MT. Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease. Blood. 2004;104:270-280.
89. Tang Y, Lu A, Aronow BJ, Sharp FR. Blood genomic responses differ after stroke, seizures, hypoglycemia, and hypoxia: blood genomic fingerprints of disease. Ann Neurol. 2001;50:699-707.
90. Bull TM, Coldren CD, Moore M, Sotto-Santiago SM, Pham DV, Nana-Sinkam SP, Voelkel NF, Geraci MW. Gene microarray analysis of peripheral blood cells in pulmonary arterial hypertension. Am J Respir Crit Care Med. 2004;170:911-919.
91. Lampe JW, Stepaniants SB, Mao M, Radich JP, Dai H, Linsley PS, Friend SH, Potter JD. Signatures of environmental exposures using peripheral leukocyte gene expression: tobacco smoke. Cancer Epidemiol Biomarkers Prev. 2004;13:445-453.