Systemic Effects of Inflammation on Health during Chronic HIV Infection

Immunity

Volumn 39, Issue 4, 2013, Pages 633-645

  Deeks, Steven G ^a   Tracy, Russell ^b   Douek, Daniel C ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VERMONT   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIINFLAMMATORY AGENT; ANTIRETROVIRUS AGENT; APIXABAN; CELECOXIB; CHLOROQUINE; CYCLOOXYGENASE 2 INHIBITOR; DABIGATRAN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GROWTH HORMONE; HYDROXYCHLOROQUINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERLEUKIN 7; ISOTRETINOIN; LEFLUNOMIDE; LENALIDOMIDE; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MESALAZINE; METFORMIN; METHOTREXATE; PREBIOTIC AGENT; PROBIOTIC AGENT; RAPAMYCIN; RIFAXIMIN; RUXOLITINIB; SEVELAMER; UNINDEXED DRUG; VALACICLOVIR; VALGANCICLOVIR;

CELL AGING; CHRONIC DISEASE; CHRONIC INFLAMMATION; DIET; DRUG EFFECT; EXERCISE; FIBROSIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERCOAGULABILITY; INFLAMMATION; INFLAMMATORY DISEASE; INTESTINE MUCOSA; LIVER FUNCTION; METABOLIC SYNDROME X; MORBIDITY; OBESITY; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW;

AGE FACTORS; ANTI-HIV AGENTS; ANTI-INFLAMMATORY AGENTS; CHRONIC DISEASE; HIV; HIV INFECTIONS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTESTINAL MUCOSA; LIVER; MODELS, IMMUNOLOGICAL; MONOCYTES; MULTIPLE ORGAN FAILURE; PROTEIN BIOSYNTHESIS; THROMBOPHILIA;

EID: 84885753789     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.10.001     Document Type: Review

References (130)

1. Abrams D., Lévy Y., Losso M.H., Babiker A., Collins G., Cooper D.A., Darbyshire J., Emery S., Fox L., Gordin F., et al. Interleukin-2 therapy in patients with HIV infection. N.Engl. J. Med. 2009, 361:1548-1559. INSIGHT-ESPRIT Study Group, SILCAAT Scientific CommitteeSILCAAT Scientific Committee.
2. Ancuta P., Kamat A., Kunstman K.J., Kim E.Y., Autissier P., Wurcel A., Zaman T., Stone D., Mefford M., Morgello S., et al. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 2008, 3:e2516.
3. Armah K.A., McGinnis K., Baker J., Gibert C., Butt A.A., Bryant K.J., Goetz M., Tracy R., Oursler K.K., Rimland D., et al. HIV status, burden of comorbid disease, and biomarkers of inflammation, altered coagulation, and monocyte activation. Clin. Infect. Dis. 2012, 55:126-136.
4. Baker J., Quick H., Hullsiek K.H., Tracy R., Duprez D., Henry K., Neaton J.D. Interleukin-6 and d-dimer levels are associated with vascular dysfunction in patients with untreated HIV infection. HIV Med. 2010, 11:608-609.
5. Baker J.V., Brummel-Ziedins K., Neuhaus J., Duprez D., Cummins N., Dalmau D., Dehovitz J., Lehmann C., Sullivan A., Woolley I., et al. HIV replication alters the composition of extrinsic pathway coagulation factors and increases thrombin generation. J.Am. Heart Assoc. 2013, 2:e000264. INSIGHT SMART Study Team.
6. Balagopal A., Philp F.H., Astemborski J., Block T.M., Mehta A., Long R., Kirk G.D., Mehta S.H., Cox A.L., Thomas D.L., Ray S.C. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology 2008, 135:226-233.
7. Balagopal A., Ray S.C., De Oca R.M., Sutcliffe C.G., Vivekanandan P., Higgins Y., Mehta S.H., Moore R.D., Sulkowski M.S., Thomas D.L., Torbenson M.S. Kupffer cells are depleted with HIV immunodeficiency and partially recovered with antiretroviral immune reconstitution. AIDS 2009, 23:2397-2404.
8. Bissuel F., Berruyer M., Causse X., Dechavanne M., Trepo C. Acquired protein S deficiency: correlation with advanced disease in HIV-1-infected patients. J.Acquir. Immune Defic. Syndr. 1992, 5:484-489.
9. Boasso A., Herbeuval J.P., Hardy A.W., Anderson S.A., Dolan M.J., Fuchs D., Shearer G.M. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood 2007, 109:3351-3359.
10. Bouchlaka M.N., Sckisel G.D., Chen M., Mirsoian A., Zamora A.E., Maverakis E., Wilkins D.E.C., Alderson K.L., Hsiao H.H., Weiss J.M., et al. Aging predisposes to acute inflammatory induced pathology after tumor immunotherapy. J.Exp. Med. 2013, Published online September 30, 2013. 10.1084/jem.20131219.
11. Boulware D.R., Hullsiek K.H., Puronen C.E., Rupert A., Baker J.V., French M.A., Bohjanen P.R., Novak R.M., Neaton J.D., Sereti I. Higher levels of CRP, D-dimer, IL-6, and hyaluronic acid before initiation of antiretroviral therapy (ART) are associated with increased risk of AIDS or death. J.Infect. Dis. 2011, 203:1637-1646. INSIGHT Study Group.
12. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., Nguyen P.L., Khoruts A., Larson M., Haase A.T., Douek D.C. CD4+ Tcell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J.Exp. Med. 2004, 200:749-759.
13. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., Kazzaz Z., Bornstein E., Lambotte O., Altmann D., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 2006, 12:1365-1371.
14. Brenchley J.M., Paiardini M., Knox K.S., Asher A.I., Cervasi B., Asher T.E., Scheinberg P., Price D.A., Hage C.A., Kholi L.M., et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008, 112:2826-2835.
15. Brummel-Ziedins K. Models for thrombin generation and risk of disease. J.Thromb. Haemost. 2013, 11(Suppl 1):212-223.
16. Burdo T.H., Soulas C., Orzechowski K., Button J., Krishnan A., Sugimoto C., Alvarez X., Kuroda M.J., Williams K.C. Increased monocyte turnover from bone marrow correlates with severity of SIV encephalitis and CD163 levels in plasma. PLoS Pathog. 2010, 6:e1000842.
17. Burdo T.H., Lentz M.R., Autissier P., Krishnan A., Halpern E., Letendre S., Rosenberg E.S., Ellis R.J., Williams K.C. Soluble CD163 made by monocyte/macrophages is a novel marker of HIV activity in early and chronic infection prior to and after anti-retroviral therapy. J.Infect. Dis. 2011, 204:154-163.
18. Burdo T.H., Lo J., Abbara S., Wei J., DeLelys M.E., Preffer F., Rosenberg E.S., Williams K.C., Grinspoon S. Soluble CD163, a novel marker of activated macrophages, is elevated and associated with noncalcified coronary plaque in HIV-infected patients. J.Infect. Dis. 2011, 204:1227-1236.
19. Buzón M.J., Massanella M., Llibre J.M., Esteve A., Dahl V., Puertas M.C., Gatell J.M., Domingo P., Paredes R., Sharkey M., et al. HIV-1 replication and immune dynamics are affected by raltegravir intensification of HAART-suppressed subjects. Nat. Med. 2010, 16:460-465.
20. Byakwaga H., Kelly M., Purcell D.F., French M.A., Amin J., Lewin S.R., Haskelberg H., Kelleher A.D., Garsia R., Boyd M.A., et al. Intensification of antiretroviral therapy with raltegravir or addition of hyperimmune bovine colostrum in HIV-infected patients with suboptimal CD4+ T-cell response: a randomized controlled trial. J.Infect. Dis. 2011, 204:1532-1540. CORAL Study Group.
21. Cahn P., Ruxrungtham K., Gazzard B., Diaz R.S., Gori A., Kotler D.P., Vriesema A., Georgiou N.A., Garssen J., Clerici M., Lange J.M. The immunomodulatory nutritional intervention NR100157 reduced CD4+ T-cell decline and immune activation: a 1-year multicenter randomized controlled double-blind trial in HIV-infected persons not receiving antiretroviral therapy (The BITE Study). Clin. Infect. Dis. 2013, 57:139-146. Blinded Nutritional Study for Immunity and Tolerance Evaluation Study Team.
22. Calmy A., Gayet-Ageron A., Montecucco F., Nguyen A., Mach F., Burger F., Ubolyam S., Carr A., Ruxungtham K., Hirschel B., Ananworanich J. HIV increases markers of cardiovascular risk: results from a randomized, treatment interruption trial. AIDS 2009, 23:929-939. STACCATO Study Group.
23. Cesari M., Penninx B.W., Newman A.B., Kritchevsky S.B., Nicklas B.J., Sutton-Tyrrell K., Tracy R.P., Rubin S.M., Harris T.B., Pahor M. Inflammatory markers and cardiovascular disease (The Health, Aging and Body Composition [Health ABC] Study). Am. J. Cardiol. 2003, 92:522-528.
24. Chevalier M.F., Petitjean G., Dunyach-Rémy C., Didier C., Girard P.M., Manea M.E., Campa P., Meyer L., Rouzioux C., Lavigne J.P., et al. The Th17/Treg ratio, IL-1RA and sCD14 levels in primary HIV infection predict the T-cell activation set point in the absence of systemic microbial translocation. PLoS Pathog. 2013, 9:e1003453.
25. Clegg A., Young J., Iliffe S., Rikkert M.O., Rockwood K. Frailty in elderly people. Lancet 2013, 381:752-762.
26. Cushman M., Lemaitre R.N., Kuller L.H., Psaty B.M., Macy E.M., Sharrett A.R., Tracy R.P. Fibrinolytic activation markers predict myocardial infarction in the elderly. The Cardiovascular Health Study. Arterioscler. Thromb. Vasc. Biol. 1999, 19:493-498.
27. Cushman M., Folsom A.R., Wang L., Aleksic N., Rosamond W.D., Tracy R.P., Heckbert S.R. Fibrin fragment D-dimer and the risk of future venous thrombosis. Blood 2003, 101:1243-1248.
28. De Martinis M., Franceschi C., Monti D., Ginaldi L. Inflamm-ageing and lifelong antigenic load as major determinants of ageing rate and longevity. FEBS Lett. 2005, 579:2035-2039.
29. Deeks S.G. HIV infection, inflammation, immunosenescence, and aging. Annu. Rev. Med. 2011, 62:141-155.
30. Deeks S.G., Kitchen C.M., Liu L., Guo H., Gascon R., Narváez A.B., Hunt P., Martin J.N., Kahn J.O., Levy J., et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 2004, 104:942-947.
31. Desquilbet L., Jacobson L.P., Fried L.P., Phair J.P., Jamieson B.D., Holloway M., Margolick J.B. HIV-1 infection is associated with an earlier occurrence of a phenotype related to frailty. J.Gerontol. A Biol. Sci. Med. Sci. 2007, 62:1279-1286. Multicenter AIDS Cohort Study.
32. Doisne J.M., Urrutia A., Lacabaratz-Porret C., Goujard C., Meyer L., Chaix M.L., Sinet M., Venet A. CD8+ Tcells specific for EBV, cytomegalovirus, and influenza virus are activated during primary HIV infection. J.Immunol. 2004, 173:2410-2418.
33. Duffield J.S., Forbes S.J., Constandinou C.M., Clay S., Partolina M., Vuthoori S., Wu S., Lang R., Iredale J.P. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J.Clin. Invest. 2005, 115:56-65.
34. Duprez D.A., Neuhaus J., Kuller L.H., Tracy R., Belloso W., De Wit S., Drummond F., Lane H.C., Ledergerber B., Lundgren J., et al. Inflammation, coagulation and cardiovascular disease in HIV-infected individuals. PLoS ONE 2012, 7:e44454. INSIGHT SMART Study Group.
35. Ellis C.L., Ma Z.M., Mann S.K., Li C.S., Wu J., Knight T.H., Yotter T., Hayes T.L., Maniar A.H., Troia-Cancio P.V., et al. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-level 16S ribosomal DNA (rDNA) quantification and correlations with immune activation. J.Acquir. Immune Defic. Syndr. 2011, 57:363-370.
36. Engelmann B., Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol. 2013, 13:34-45.
37. Estes J.D., Harris L.D., Klatt N.R., Tabb B., Pittaluga S., Paiardini M., Barclay G.R., Smedley J., Pung R., Oliveira K.M., et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 2010, 6:e1001052.
38. Favre D., Mold J., Hunt P.W., Kanwar B., Loke P., Seu L., Barbour J.D., Lowe M.M., Jayawardene A., Aweeka F., et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory Tcells in HIV disease. Sci. Transl. Med. 2010, 2. 32ra36.
39. Fernandez S., Tanaskovic S., Helbig K., Rajasuriar R., Kramski M., Murray J.M., Beard M., Purcell D., Lewin S.R., Price P., French M.A. CD4+ T-cell deficiency in HIV patients responding to antiretroviral therapy is associated with increased expression of interferon-stimulated genes in CD4+ Tcells. J.Infect. Dis. 2011, 204:1927-1935.
40. Finch C.E. The Biology of Human Longevity 2007, Elsevier, Amsterdam.
41. Ford E.S., Greenwald J.H., Richterman A.G., Rupert A., Dutcher L., Badralmaa Y., Natarajan V., Rehm C., Hadigan C., Sereti I. Traditional risk factors and D-dimer predict incident cardiovascular disease events in chronic HIV infection. AIDS 2010, 24:1509-1517.
42. Freiberg M.S., Chang C.C., Kuller L.H., Skanderson M., Lowy E., Kraemer K.L., Butt A.A., Bidwell Goetz M., Leaf D., Oursler K.A., et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern. Med. 2013, 173:614-622.
43. French M.A., King M.S., Tschampa J.M., da Silva B.A., Landay A.L. Serum immune activation markers are persistently increased in patients with HIV infection after 6 years of antiretroviral therapy despite suppression of viral replication and reconstitution of CD4+ Tcells. J.Infect. Dis. 2009, 200:1212-1215.
44. French A.L., Evans C.T., Agniel D.M., Cohen M.H., Peters M., Landay A.L., Desai S.N. Microbial translocation and liver disease progression in women coinfected with HIV and hepatitis C virus. J.Infect. Dis. 2013, 208:679-689.
45. Fultz S.L., McGinnis K.A., Skanderson M., Ragni M.V., Justice A.C. Association of venous thromboembolism with human immunodeficiency virus and mortality in veterans. Am. J. Med. 2004, 116:420-423.
46. Funderburg N.T., Mayne E., Sieg S.F., Asaad R., Jiang W., Kalinowska M., Luciano A.A., Stevens W., Rodriguez B., Brenchley J.M., et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to invivo coagulation and immune activation. Blood 2010, 115:161-167.
47. Ganesan A., Crum-Cianflone N., Higgins J., Qin J., Rehm C., Metcalf J., Brandt C., Vita J., Decker C.F., Sklar P., et al. High dose atorvastatin decreases cellular markers of immune activation without affecting HIV-1 RNA levels: results of a double-blind randomized placebo controlled clinical trial. J.Infect. Dis. 2011, 203:756-764.
48. Gori A., Tincati C., Rizzardini G., Torti C., Quirino T., Haarman M., Ben Amor K., van Schaik J., Vriesema A., Knol J., et al. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J.Clin. Microbiol. 2008, 46:757-758.
49. Gori A., Rizzardini G., Van't Land B., Amor K.B., van Schaik J., Torti C., Quirino T., Tincati C., Bandera A., Knol J., et al. Specific prebiotics modulate gut microbiota and immune activation in HAART-naive HIV-infected adults: results of the "COPA" pilot randomized trial. Mucosal Immunol. 2011, 4:554-563.
50. Handley S.A., Thackray L.B., Zhao G., Presti R., Miller A.D., Droit L., Abbink P., Maxfield L.F., Kambal A., Duan E., et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 2012, 151:253-266.
51. Hasegawa A., Liu H., Ling B., Borda J.T., Alvarez X., Sugimoto C., Vinet-Oliphant H., Kim W.K., Williams K.C., Ribeiro R.M., et al. The level of monocyte turnover predicts disease progression in the macaque model of AIDS. Blood 2009, 114:2917-2925.
52. Hatano H., Jain V., Hunt P.W., Lee T.H., Sinclair E., Do T.D., Hoh R., Martin J.N., McCune J.M., Hecht F., et al. Cell-based measures of viral persistence are associated with immune activation and programmed cell death protein 1 (PD-1)-expressing CD4+ Tcells. J.Infect. Dis. 2013, 208:50-56.
53. Hatano H., Strain M.C., Scherzer R., Bacchetti P., Wentworth D., Hoh R., Martin J.N., McCune J.M., Neaton J.D., Tracy R., et al. Increase in 2-LTR circles and decrease in D-dimer after raltegravir intensification in treated HIV-infected patients: a randomized, placebo-controlled trial. J.Infect. Dis. 2013, Published online September 18, 2013. 10.1093/infdis/jit453.
54. Herbeuval J.P., Shearer G.M. HIV-1 immunopathogenesis: how good interferon turns bad. Clin. Immunol. 2007, 123:121-128.
55. Hileman C.O., Longenecker C.T., Carman T.L., Milne G.L., Labbato D.E., Storer N.J., White C.A., McComsey G.A. Elevated D-dimer is independently associated with endothelial dysfunction: a cross-sectional study in HIV-infected adults on antiretroviral therapy. Antivir. Ther. (Lond.) 2012, 17:1345-1349.
56. Hunt P.W., Martin J.N., Sinclair E., Bredt B., Hagos E., Lampiris H., Deeks S.G. T cell activation is associated with lower CD4+ Tcell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J.Infect. Dis. 2003, 187:1534-1543.
57. Hunt P.W., Martin J.N., Sinclair E., Epling L., Teague J., Jacobson M.A., Tracy R.P., Corey L., Deeks S.G. Valganciclovir reduces Tcell activation in HIV-infected individuals with incomplete CD4+ Tcell recovery on antiretroviral therapy. J.Infect. Dis. 2011, 203:1474-1483.
58. Hunt P.W., Shulman N.S., Hayes T.L., Dahl V., Somsouk M., Funderburg N.T., McLaughlin B., Landay A.L., Adeyemi O., Gilman L.E., et al. The immunologic effects of maraviroc intensification in treated HIV-infected individuals with incomplete CD4+ T-cell recovery: a randomized trial. Blood 2013, 121:4635-4646.
59. Jiang W., Lederman M.M., Hunt P., Sieg S.F., Haley K., Rodriguez B., Landay A., Martin J., Sinclair E., Asher A.I., et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J.Infect. Dis. 2009, 199:1177-1185.
60. Jong E., Louw S., Meijers J.C., de Kruif M.D., ten Cate H., Büller H.R., Mulder J.W., van Gorp E.C. The hemostatic balance in HIV-infected patients with and without antiretroviral therapy: partial restoration with antiretroviral therapy. AIDS Patient Care STDS 2009, 23:1001-1007.
61. Jong E., Louw S., van Gorp E.C., Meijers J.C., ten Cate H., Jacobson B.F. The effect of initiating combined antiretroviral therapy on endothelial cell activation and coagulation markers in South African HIV-infected individuals. Thromb. Haemost. 2010, 104:1228-1234.
62. Justice A.C. HIV and aging: time for a new paradigm. Curr. HIV/AIDS Rep. 2010, 7:69-76.
63. Justice A., Sullivan L., Fiellin D. HIV/AIDS, comorbidity, and alcohol. Alcohol Res. Health 2010, 33:258-266.
64. Justice A.C., Freiberg M.S., Tracy R., Kuller L., Tate J.P., Goetz M.B., Fiellin D.A., Vanasse G.J., Butt A.A., Rodriguez-Barradas M.C., et al. Does an index composed of clinical data reflect effects of inflammation, coagulation, and monocyte activation on mortality among those aging with HIV?. Clin. Infect. Dis. 2012, 54:984-994. VACS Project Team.
65. Kanneganti T.D., Lamkanfi M., Núñez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007, 27:549-559.
66. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
67. Kelesidis T., Kendall M.A., Yang O.O., Hodis H.N., Currier J.S. Biomarkers of microbial translocation and macrophage activation: association with progression of subclinical atherosclerosis in HIV-1 infection. J.Infect. Dis. 2012, 206:1558-1567.
68. Klatt N.R., Canary L.A., Sun X., Vinton C.L., Funderburg N.T., Morcock D.R., Quiñones M., Deming C.B., Perkins M., Hazuda D.J., et al. Probiotic/prebiotic supplementation of antiretrovirals improves gastrointestinal immunity in SIV-infected macaques. J.Clin. Invest. 2013, 123:903-907.
69. Klatt N.R., Chomont N., Douek D.C., Deeks S.G. Immune activation and HIV persistence: implications for curative approaches to HIV infection. Immunol. Rev. 2013, 254:326-342.
70. Koch S., Larbi A., Ozcelik D., Solana R., Gouttefangeas C., Attig S., Wikby A., Strindhall J., Franceschi C., Pawelec G. Cytomegalovirus infection: a driving force in human Tcell immunosenescence. Ann. N Y Acad. Sci. 2007, 1114:23-35.
71. Koeth R.A., Wang Z., Levison B.S., Buffa J.A., Org E., Sheehy B.T., Britt E.B., Fu X., Wu Y., Li L., et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 2013, 19:576-585.
72. Kuller L.H., Tracy R., Belloso W., De Wit S., Drummond F., Lane H.C., Ledergerber B., Lundgren J., Neuhaus J., Nixon D., et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 2008, 5:e203. INSIGHT SMART Study Group.
73. Lassenius M.I., Pietiläinen K.H., Kaartinen K., Pussinen P.J., Syrjänen J., Forsblom C., Pörsti I., Rissanen A., Kaprio J., Mustonen J., et al. Bacterial endotoxin activity in human serum is associated with dyslipidemia, insulin resistance, obesity, and chronic inflammation. Diabetes Care 2011, 34:1809-1815. FinnDiane Study Group.
74. Ledwaba L., Tavel J.A., Khabo P., Maja P., Qin J., Sangweni P., Liu X., Follmann D., Metcalf J.A., Orsega S., et al. Pre-ART levels of inflammation and coagulation markers are strong predictors of death in a South African cohort with advanced HIV disease. PLoS ONE 2012, 7:e24243. Project Phidisa Biomarkers Team.
75. Li Q., Duan L., Estes J.D., Ma Z.M., Rourke T., Wang Y., Reilly C., Carlis J., Miller C.J., Haase A.T. Peak SIV replication in resting memory CD4+ Tcells depletes gut lamina propria CD4+ Tcells. Nature 2005, 434:1148-1152.
76. Li L., Deng X., Linsuwanon P., Bangsberg D., Bwana M.B., Hunt P., Martin J.N., Deeks S.G., Delwart E. AIDS alters the commensal plasma virome. J.Virol. 2013, 87:10912-10915.
77. Libby P., Ridker P.M., Hansson G.K. Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
78. Lijfering W.M., Sprenger H.G., Georg R.R., van der Meulen P.A., van der Meer J. Relationship between progression to AIDS and thrombophilic abnormalities in HIV infection. Clin. Chem. 2008, 54:1226-1233.
79. Lok J.J., Hunt P.W.o., Collier A.C., Benson C.A., Witt M.D., Luque A.E., Deeks S.G., Bosch R.J. The impact of age on the prognostic capacity of CD8+ T-cell activation during suppressive antiretroviral therapy. AIDS 2013, Published online August 24, 2013. 10.1097/QAD.0b013e32836191b1.
80. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
81. Marchetti G., Cozzi-Lepri A., Merlini E., Bellistrì G.M., Castagna A., Galli M., Verucchi G., Antinori A., Costantini A., Giacometti A., et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4+ cell count. AIDS 2011, 25:1385-1394. ICONA Foundation Study Group.
82. Mavigner M., Cazabat M., Dubois M., L'Faqihi F.E., Requena M., Pasquier C., Klopp P., Amar J., Alric L., Barange K., et al. Altered CD4+ Tcell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J.Clin. Invest. 2012, 122:62-69.
83. Mehandru S., Poles M.A., Tenner-Racz K., Horowitz A., Hurley A., Hogan C., Boden D., Racz P., Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J.Exp. Med. 2004, 200:761-770.
84. Mehandru S., Poles M.A., Tenner-Racz K., Jean-Pierre P., Manuelli V., Lopez P., Shet A., Low A., Mohri H., Boden D., et al. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med. 2006, 3:e484.
85. Monte S.V., Caruana J.A., Ghanim H., Sia C.L., Korzeniewski K., Schentag J.J., Dandona P. Reduction in endotoxemia, oxidative and inflammatory stress, and insulin resistance after Roux-en-Y gastric bypass surgery in patients with morbid obesity and type 2 diabetes mellitus. Surgery 2012, 151:587-593.
86. Moore R.D., Bartlett J.G., Gallant J.E. Association between use of HMG CoA reductase inhibitors and mortality in HIV-infected patients. PLoS ONE 2011, 6:e21843.
87. Musselwhite L.W., Sheikh V., Norton T.D., Rupert A., Porter B.O., Penzak S.R., Skinner J., Mican J.M., Hadigan C., Sereti I. Markers of endothelial dysfunction, coagulation and tissue fibrosis independently predict venous thromboembolism in HIV. AIDS 2011, 25:787-795.
88. Naeger D.M., Martin J.N., Sinclair E., Hunt P.W., Bangsberg D.R., Hecht F., Hsue P., McCune J.M., Deeks S.G. Cytomegalovirus-specific Tcells persist at very high levels during long-term antiretroviral treatment of HIV disease. PLoS ONE 2010, 5:e8886.
89. Nalle S.C., Turner J.R. Endothelial and epithelial barriers in graft-versus-host disease. Adv. Exp. Med. Biol. 2012, 763:105-131.
90. Nesheim M.E., Tracy R.P., Mann K.G. "Clotspeed," a mathematical simulation of the functional properties of prothrombinase. J.Biol. Chem. 1984, 259:1447-1453.
91. Neuhaus J., Jacobs D.R., Baker J.V., Calmy A., Duprez D., La Rosa A., Kuller L.H., Pett S.L., Ristola M., Ross M.J., et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J.Infect. Dis. 2010, 201:1788-1795.
92. O'Brien M., Montenont E., Hu L., Nardi M.A., Valdes V., Merolla M., Gettenberg G., Cavanagh K., Aberg J.A., Bhardwaj N., Berger J.S. Aspirin attenuates platelet activation and immune activation in HIV-1-infected subjects on antiretroviral therapy: a pilot study. J.Acquir. Immune Defic. Syndr. 2013, 63:280-288.
93. Palella F.J., Gange S.J., Benning L., Jacobson L., Kaplan R.C., Landay A.L., Tracy R.P., Elion R. Inflammatory biomarkers and abacavir use in the Women's Interagency HIV Study and the Multicenter AIDS Cohort Study. AIDS 2010, 24:1657-1665.
94. Pandrea I., Cornell E., Wilson C., Ribeiro R.M., Ma D., Kristoff J., Xu C., Haret-Richter G.S., Trichel A., Apetrei C., et al. Coagulation biomarkers predict disease progression in SIV-infected nonhuman primates. Blood 2012, 120:1357-1366.
95. Papagno L., Spina C.A., Marchant A., Salio M., Rufer N., Little S., Dong T., Chesney G., Waters A., Easterbrook P., et al. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol. 2004, 2:E20.
96. Paton N.I., Goodall R.L., Dunn D.T., Franzen S., Collaco-Moraes Y., Gazzard B.G., Williams I.G., Fisher M.J., Winston A., Fox J., et al. Effects of hydroxychloroquine on immune activation and disease progression among HIV-infected patients not receiving antiretroviral therapy: a randomized controlled trial. JAMA 2012, 308:353-361. Hydroxychloroquine Trial Team.
97. Peters L., Neuhaus J., Mocroft A., Soriano V., Rockstroh J., Dore G., Puoti M., Tedaldi E., Clotet B., Kupfer B., et al. Hyaluronic acid levels predict increased risk of non-AIDS death in hepatitis-coinfected persons interrupting antiretroviral therapy in the SMART Study. Antivir. Ther. (Lond.) 2011, 16:667-675. SMART Study Group.
98. Pettersen F.O., Torheim E.A., Dahm A.E., Aaberge I.S., Lind A., Holm M., Aandahl E.M., Sandset P.M., Taskén K., Kvale D. An exploratory trial of cyclooxygenase type 2 inhibitor in HIV-1 infection: downregulated immune activation and improved Tcell-dependent vaccine responses. J.Virol. 2011, 85:6557-6566.
99. Piconi S., Parisotto S., Rizzardini G., Passerini S., Terzi R., Argenteri B., Meraviglia P., Capetti A., Biasin M., Trabattoni D., Clerici M. Hydroxychloroquine drastically reduces immune activation in HIV-infected, antiretroviral therapy-treated immunologic nonresponders. Blood 2011, 118:3263-3272.
100. Pindel A., Sadler A. The role of protein kinase R in the interferon response. J.Interferon Cytokine Res. 2011, 31:59-70.
101. Pussinen P.J., Tuomisto K., Jousilahti P., Havulinna A.S., Sundvall J., Salomaa V. Endotoxemia, immune response to periodontal pathogens, and systemic inflammation associate with incident cardiovascular disease events. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1433-1439.
102. Pussinen P.J., Havulinna A.S., Lehto M., Sundvall J., Salomaa V. Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care 2011, 34:392-397.
103. Redd A.D., Dabitao D., Bream J.H., Charvat B., Laeyendecker O., Kiwanuka N., Lutalo T., Kigozi G., Tobian A.A., Gamiel J., et al. Microbial translocation, the innate cytokine response, and HIV-1 disease progression in Africa. Proc. Natl. Acad. Sci. USA 2009, 106:6718-6723.
104. Rivera C.A., Bradford B.U., Hunt K.J., Adachi Y., Schrum L.W., Koop D.R., Burchardt E.R., Rippe R.A., Thurman R.G. Attenuation of CCl(4)-induced hepatic fibrosis by GdCl(3) treatment or dietary glycine. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281:G200-G207.
105. Rotger M., Dalmau J., Rauch A., McLaren P., Bosinger S.E., Martinez R., Sandler N.G., Roque A., Liebner J., Battegay M., et al. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J.Clin. Invest. 2011, 121:2391-2400.
106. Sandler N.G., Koh C., Roque A., Eccleston J.L., Siegel R.B., Demino M., Kleiner D.E., Deeks S.G., Liang T.J., Heller T., Douek D.C. Host response to translocated microbial products predicts outcomes of patients with HBV or HCV infection. Gastroenterology 2011, 141:1220-1230. e1-e3.
107. Sandler N.G., Wand H., Roque A., Law M., Nason M.C., Nixon D.E., Pedersen C., Ruxrungtham K., Lewin S.R., Emery S., et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J.Infect. Dis. 2011, 203:780-790. INSIGHT SMART Study Group.
108. Sankaran S., George M.D., Reay E., Guadalupe M., Flamm J., Prindiville T., Dandekar S. Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J.Virol. 2008, 82:538-545.
109. Schacker T.W., Nguyen P.L., Beilman G.J., Wolinsky S., Larson M., Reilly C., Haase A.T. Collagen deposition in HIV-1 infected lymphatic tissues and Tcell homeostasis. J.Clin. Invest. 2002, 110:1133-1139.
110. Seki E., De Minicis S., Osterreicher C.H., Kluwe J., Osawa Y., Brenner D.A., Schwabe R.F. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 2007, 13:1324-1332.
111. Shen Y.M., Frenkel E.P. Thrombosis and a hypercoagulable state in HIV-infected patients. Clin. Appl. Thromb. Hemost. 2004, 10:277-280.
112. Singh T., Newman A.B. Inflammatory markers in population studies of aging. Ageing Res. Rev. 2011, 10:319-329.
113. Smith M.Z., Bastidas S., Karrer U., Oxenius A. Impact of antigen specificity on CD4+ Tcell activation in chronic HIV-1 infection. BMC Infect. Dis. 2013, 13:100.
114. Stacey A.R., Norris P.J., Qin L., Haygreen E.A., Taylor E., Heitman J., Lebedeva M., DeCamp A., Li D., Grove D., et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J.Virol. 2009, 83:3719-3733.
115. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., Schreiber R.D. How cells respond to interferons. Annu. Rev. Biochem. 1998, 67:227-264.
116. Su G.L. Lipopolysaccharides in liver injury: molecular mechanisms of Kupffer cell activation. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283:G256-G265.
117. Sylwester A.W., Mitchell B.L., Edgar J.B., Taormina C., Pelte C., Ruchti F., Sleath P.R., Grabstein K.H., Hosken N.A., Kern F., et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ Tcells dominate the memory compartments of exposed subjects. J.Exp. Med. 2005, 202:673-685.
118. Tang W.H., Wang Z., Levison B.S., Koeth R.A., Britt E.B., Fu X., Wu Y., Hazen S.L. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N.Engl. J. Med. 2013, 368:1575-1584.
119. Tien P.C., Choi A.I., Zolopa A.R., Benson C., Tracy R., Scherzer R., Bacchetti P., Shlipak M., Grunfeld C. Inflammation and mortality in HIV-infected adults: analysis of the FRAM study cohort. J.Acquir. Immune Defic. Syndr. 2010, 55:316-322.
120. Tran L., Greenwood-Van Meerveld B. Age-associated remodeling of the intestinal epithelial barrier. J.Gerontol. A Biol. Sci. Med. Sci. 2013, 68:1045-1056.
121. Tripodi A., Mannucci P.M. The coagulopathy of chronic liver disease. N.Engl. J. Med. 2011, 365:147-156.
122. Tuyama A.C., Hong F., Saiman Y., Wang C., Ozkok D., Mosoian A., Chen P., Chen B.K., Klotman M.E., Bansal M.B. Human immunodeficiency virus (HIV)-1 infects human hepatic stellate cells and promotes collagen I and monocyte chemoattractant protein-1 expression: implications for the pathogenesis of HIV/hepatitis C virus-induced liver fibrosis. Hepatology 2010, 52:612-622.
123. Undas A., Brummel-Ziedins K.E., Mann K.G. Statins and blood coagulation. Arterioscler. Thromb. Vasc. Biol. 2005, 25:287-294.
124. Vasto S., Candore G., Balistreri C.R., Caruso M., Colonna-Romano G., Grimaldi M.P., Listi F., Nuzzo D., Lio D., Caruso C. Inflammatory networks in ageing, age-related diseases and longevity. Mech. Ageing Dev. 2007, 128:83-91.
125. Vujkovic-Cvijin I., Dunham R.M., Iwai S., Maher M.C., Albright R.G., Broadhurst M.J., Hernandez R.D., Lederman M.M., Huang Y., Somsouk M., et al. Dysbiosis of the gut microbiota is associated with hiv disease progression and tryptophan catabolism. Sci. Transl. Med. 2013, 5. 93ra91.
126. Walston J., McBurnie M.A., Newman A., Tracy R.P., Kop W.J., Hirsch C.H., Gottdiener J., Fried L.P. Frailty and activation of the inflammation and coagulation systems with and without clinical comorbidities: results from the Cardiovascular Health Study. Arch. Intern. Med. 2002, 162:2333-2341. Cardiovascular Health Study.
127. Weber R., Sabin C.A., Friis-Møller N., Reiss P., El-Sadr W.M., Kirk O., Dabis F., Law M.G., Pradier C., De Wit S., et al. Liver-related deaths in persons infected with the human immunodeficiency virus: the D:A:D study. Arch. Intern. Med. 2006, 166:1632-1641.
128. Wittkop L., Bitard J., Lazaro E., Neau D., Bonnet F., Mercie P., Dupon M., Hessamfar M., Ventura M., Malvy D., et al. Effect of cytomegalovirus-induced immune response, self antigen-induced immune response, and microbial translocation on chronic immune activation in successfully treated HIV type 1-infected patients: the ANRS CO3 Aquitaine Cohort. J.Infect. Dis. 2013, 207:622-627. Groupe d'Epidémiologie Clinique du SIDA en Aquitaine.
129. Woollard K.J., Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol. 2010, 7:77-86.
130. Zeng M., Southern P.J., Reilly C.S., Beilman G.J., Chipman J.G., Schacker T.W., Haase A.T. Lymphoid tissue damage in HIV-1 infection depletes naïve Tcells and limits Tcell reconstitution after antiretroviral therapy. PLoS Pathog. 2012, 8:e1002437.