Effect of probiotic supplement on cytokine levels in HIV-infected individuals: A preliminary study

Nutrients

Volumn 7, Issue 10, 2015, Pages 8335-8347

  Falasca, Katia ^a   Vecchiet, Jacopo ^a   Ucciferri, Claudio ^a   di Nicola, Marta ^a   D’Angelo, Chiara ^a   Reale, Marcella ^a  

^a UNIVERSITY OF CHIETI   (Italy)

Author keywords

AIDS; ART; Dietary supplements; Inflammation; Lactobacillus casei shirota; Nutrition

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ANTIRETROVIRUS AGENT; ASPARTATE AMINOTRANSFERASE; C REACTIVE PROTEIN; CD4 ANTIBODY; CD56 ANTIGEN; CD8 ANTIGEN; CHOLESTEROL; CREATININE; CYSTATIN C; CYTOKINE; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 23; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; NITROGEN; PROBIOTIC AGENT; TRANSFORMING GROWTH FACTOR BETA; TRIACYLGLYCEROL; UREA; ANTIINFLAMMATORY AGENT;

ADULT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CARDIOVASCULAR RISK; CELL COUNT; CLINICAL ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE SEDIMENTATION RATE; HEMATOLOGICAL PARAMETERS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGICAL PARAMETERS; MALE; MICROALBUMINURIA; OPEN STUDY; PROSPECTIVE STUDY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SELF EVALUATION; STRUCTURED QUESTIONNAIRE; T LYMPHOCYTE; TH1 TH2 BALANCE; VIRUS LOAD; BLOOD; FERMENTED MILK PRODUCT; GENETICS; HIV INFECTIONS; IMMUNOLOGY; LACTOBACILLUS CASEI; LYMPHOCYTE COUNT;

ANTI-INFLAMMATORY AGENTS; ANTI-RETROVIRAL AGENTS; ANTIGENS, CD56; CULTURED MILK PRODUCTS; CYTOKINES; HIV INFECTIONS; HUMANS; INTERLEUKIN-10; INTERLEUKIN-12; LACTOBACILLUS CASEI; LYMPHOCYTE COUNT; MALE; PROBIOTICS; RNA, MESSENGER; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84942886725     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7105396     Document Type: Article

References (62)

1. Pirs, M.; Jug, B.; Erzen, B.; Sabovic, M.; Karner, P.; Poljak, M.; Tomazic, J. Cardiovascular risk assessment in HIV-infected male patients: A comparison of framingham, score, procam and dad risk equations. Acta Dermatovenerol. Alp. Pannonica Adriat. 2014, 23, 43-47. [PubMed]
2. Falasca, K.; Ucciferri, C.; Manzoli, L.; Mancino, P.; Pizzigallo, E.; Conti, P.; Vecchiet, J. Metabolic syndrome and cardiovascular risk in HIV-infected patients with lipodystrophy. Int. J. Immunopathol. Pharmacol. 2007, 20, 519-527. [PubMed]
3. Teofili, L.; Iachininoto, M.G.; Capodimonti, S.; Ucciferri, C.; Nuzzolo, E.R.; Martini, M.; Torti, L.; Falasca, K.; Vecchiet, J.; Leone, G.; et al. Endothelial progenitor cell trafficking in human immunodeficiency virus-infected persons. AIDS 2010, 24, 2443-2450. [CrossRef] [PubMed]
4. Maldarelli, F.; Palmer, S.; King, M.S.; Wiegand, A.; Polis, M.A.; Mican, J.; Kovacs, J.A.; Davey, R.T.; Rock-Kress, D.; Dewar, R.; et al. ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog. 2007, 3, e46. [CrossRef] [PubMed]
5. Zaaqoq, A.M.; Khasawneh, F.A.; Smalligan, R.D. Cardiovascular complications of HIV-associated immune dysfunction. Cardiol. Res. Pract. 2015, 2015, 302638. [CrossRef] [PubMed]
6. 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. [CrossRef] [PubMed]
7. 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+ T cell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J. Clin. Investig. 2012, 122, 62-69. [CrossRef] [PubMed]
8. Katsikis, P.D.; Mueller, Y.M.; Villinger, F. The cytokine network of acute HIV infection: A promising target for vaccines and therapy to reduce viral set-point? PLoS Pathog. 2011, 7, e1002055. [CrossRef] [PubMed]
9. Veazey, R.S.; DeMaria, M.; Chalifoux, L.V.; Shvetz, D.E.; Pauley, D.R.; Knight, H.L.; Rosenzweig, M.; Johnson, R.P.; Desrosiers, R.C.; Lackner, A.A. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998, 280, 427-431. [CrossRef] [PubMed]
10. Hummelen, R.; Vos, A.P.; van't Land, B.; van Norren, K.; Reid, G. Altered host-microbe interaction in HIV: A target for intervention with pro-and prebiotics. Int. Rev. Immunol. 2010, 29, 485-513. [CrossRef] [PubMed]
11. Cassol, E.; Malfeld, S.; Mahasha, P.; van der Merwe, S.; Cassol, S.; Seebregts, C.; Alfano, M.; Poli, G.; Rossouw, T. Persistent microbial translocation and immune activation in HIV-1-infected south africans receiving combination antiretroviral therapy. J. Infect. Dis. 2010, 202, 723-733. [PubMed]
12. Buzon, 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. [CrossRef] [PubMed]
13. 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+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 2005, 202, 673-685. [CrossRef] [PubMed]
14. 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. [CrossRef] [PubMed]
15. Kekkonen, R.A.; Lummela, N.; Karjalainen, H.; Latvala, S.; Tynkkynen, S.; Jarvenpaa, S.; Kautiainen, H.; Julkunen, I.; Vapaatalo, H.; Korpela, R. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J. Gastroenterol. 2008, 14, 2029-2036. [CrossRef] [PubMed]
16. Matsumoto, K.; Takada, T.; Shimizu, K.; Moriyama, K.; Kawakami, K.; Hirano, K.; Kajimoto, O.; Nomoto, K. Effects of a probiotic fermented milk beverage containing lactobacillus casei strain shirota on defecation frequency, intestinal microbiota, and the intestinal environment of healthy individuals with soft stools. J. Biosci. Bioeng. 2010, 110, 547-552. [CrossRef] [PubMed]
17. Reale, M.; Boscolo, P.; Bellante, V.; Tarantelli, C.; Di Nicola, M.; Forcella, L.; Li, Q.; Morimoto, K.; Muraro, R. Daily intake of lactobacillus casei shirota increases natural killer cell activity in smokers. Br. J. Nutr. 2012, 108, 308-314. [CrossRef] [PubMed]
18. Dong, H.; Rowland, I.; Thomas, L.V.; Yaqoob, P. Immunomodulatory effects of a probiotic drink containing Lactobacillus casei Shirota in healthy older volunteers. Eur. J. Nutr. 2013, 52, 1853-1863. [CrossRef] [PubMed]
19. Shida, K.; Nanno, M.; Nagata, S. Flexible cytokine production by macrophages and T cells in response to probiotic bacteria: A possible mechanism by which probiotics exert multifunctional immune regulatory activities. Gut Microbes 2011, 2, 109-114. [CrossRef] [PubMed]
20. Takeda, K.; Suzuki, T.; Shimada, S.I.; Shida, K.; Nanno, M.; Okumura, K. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei shirota. Clin. Exp. Immunol. 2006, 146, 109-115. [CrossRef] [PubMed]
21. Osborn, L.; Kunkel, S.; Nabel, G.J. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor κB. Proc. Natl. Acad. Sci. USA 1989, 86, 2336-2340. [CrossRef] [PubMed]
22. Schnittman, S.M.; Singer, K.H.; Greenhouse, J.J.; Stanley, S.K.; Whichard, L.P.; Le, P.T.; Haynes, B.F.; Fauci, A.S. Thymic microenvironment induces HIV expression. Physiologic secretion of IL-6 by thymic epithelial cells up-regulates virus expression in chronically infected cells. J. Immunol. 1991, 147, 2553-2558. [PubMed]
23. Amadori, A.; Zamarchi, R.; Veronese, M.L.; Panozzo, M.; Barelli, A.; Borri, A.; Sironi, M.; Colotta, F.; Mantovani, A.; Chieco-Bianchi, L. B cell activation during HIV-1 infection. II. Cell-to-cell interactions and cytokine requirement. J. Immunol. 1991, 146, 57-62. [PubMed]
24. Barqasho, B.; Nowak, P.; Tjernlund, A.; Kinloch, S.; Goh, L.E.; Lampe, F.; Fisher, M.; Andersson, J.; Sonnerborg, A. Kinetics of plasma cytokines and chemokines during primary HIV-1 infection and after analytical treatment interruption. HIV Med. 2009, 10, 94-102. [CrossRef] [PubMed]
25. Resino, S.; Bellon, J.M.; Sanchez-Ramon, S.; Gurbindo, D.; Munoz-Fernandez, M.A. Clinical relevance of cytokine production in HIV-1 infection in children on antiretroviral therapy. Scand. J. Immunol. 2000, 52, 634-640. [CrossRef] [PubMed]
26. Appay, V.; Sauce, D. Immune activation and inflammation in HIV-1 infection: Causes and consequences. J. Pathol. 2008, 214, 231-241. [CrossRef] [PubMed]
27. Ucciferri, C.; Falasca, K.; Vignale, F.; Di Nicola, M.; Pizzigallo, E.; Vecchiet, J. Improved metabolic profile after switch to darunavir/ritonavir in HIV positive patients previously on protease inhibitor therapy. J. Med. Virol. 2013, 85, 755-759. [CrossRef] [PubMed]
28. Vecchiet, J.; Ucciferri, C.; Falasca, K.; Mancino, P.; Di Iorio, A.; De Caterina, R. Antihypertensive and metabolic effects of telmisartan in hypertensive HIV-positive patients. Antivir. Ther. 2011, 16, 639-645. [CrossRef] [PubMed]
29. Falasca, K.; Ucciferri, C.; Mancino, P.; Di Iorio, A.; Vignale, F.; Pizzigallo, E.; Vecchiet, J. Cystatin C, adipokines and cardiovascular risk in HIV infected patients. Curr. HIV Res. 2010, 8, 405-410. [CrossRef] [PubMed]
30. Ciccarelli, N.; Fabbiani, M.; Grima, P.; Falasca, K.; Tana, M.; Baldonero, E.; Colafigli, M.; Silveri, M.C.; Vecchiet, J.; Cauda, R.; et al. Comparison of cognitive performance in HIV or HCV mono-infected and HIV-HCV co-infected patients. Infection 2013, 41, 1103-1109. [CrossRef] [PubMed]
31. Falasca, K.; Ucciferri, C.; Mancino, P.; Pizzigallo, E.; Calza, L.; Vecchiet, J. Severe HIV-associated hypertriglyceridaemia treated with rosuvastatin plus omega-3 fatty acids. Int. J. STD AIDS 2009, 20, 580-581. [CrossRef] [PubMed]
32. Ucciferri, C.; Falasca, K.; Mancino, P.; Di Iorio, A.; Vecchiet, J. Microalbuminuria and hypertension in HIV-infected patients: A preliminary study of telmisartan. Eur. Rev. Med. Pharmacol. Sci. 2012, 16, 491-498. [PubMed]
33. Falasca, K.; Ucciferri, C.; Di Nicola, M.; Vignale, F.; Di Biase, J.; Vecchiet, J. Different strategies of 25OH vitamin D supplementation in HIV-positive subjects. Int. J. STD AIDS 2014, 25, 785-792. [CrossRef] [PubMed]
34. Schacker, T.; Zeh, J.; Hu, H.; Shaughnessy, M.; Corey, L. Changes in plasma human immunodeficiency virus type 1 RNA associated with herpes simplex virus reactivation and suppression. J. Infect. Dis. 2002, 186, 1718-1725. [CrossRef]
35. 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.; et al. 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. [CrossRef] [PubMed]
36. Hummelen, R.; Changalucha, J.; Butamanya, N.L.; Koyama, T.E.; Cook, A.; Habbema, J.D.; Reid, G. Effect of 25 weeks probiotic supplementation on immune function of HIV patients. Gut Microbes 2011, 2, 80-85. [CrossRef] [PubMed]
37. Helwig, U.; Lammers, K.M.; Rizzello, F.; Brigidi, P.; Rohleder, V.; Caramelli, E.; Gionchetti, P.; Schrezenmeir, J.; Foelsch, U.R.; Schreiber, S.; et al. Lactobacilli, bifidobacteria and E. coli nissle induce pro-and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J. Gastroenterol. 2006, 12, 5978-5986. [PubMed]
38. Klein, A.; Friedrich, U.; Vogelsang, H.; Jahreis, G. Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. Eur. J. Clin. Nutr. 2008, 62, 584-593. [CrossRef] [PubMed]
39. Liu, J.E.; Zhang, Y.; Zhang, J.; Dong, P.L.; Chen, M.; Duan, Z.P. Probiotic yogurt effects on intestinal flora of patients with chronic liver disease. Nurs. Res. 2010, 59, 426-432. [CrossRef] [PubMed]
40. Baken, K.A.; Pennings, J.L.; de Vries, A.; Breit, T.M.; van Steeg, H.; van Loveren, H. Gene expression profiling of Bis(tri-n-butyltin)oxide (TBTO)-induced immunotoxicity in mice and rats. J. Immunotoxicol. 2006, 3, 227-244. [CrossRef] [PubMed]
41. Kekow, J.;Wachsman, W.; McCutchan, J.A.; Gross, W.L.; Zachariah, M.; Carson, D.A.; Lotz, M. Transforming growth factor-beta and suppression of humoral immune responses in HIV infection. J. Clin. Investig. 1991, 87, 1010-1016. [CrossRef]
42. Futh, R.; Herder, C.; Forster, S.; Muller-Scholze, S.; Kruse, N.; Rieckmann, P.; Heinig, A.; Koenig, W.; Scherbaum, W.A.; Kolb, H.; et al. Evaluation of diagnostic relevance of mrna levels in peripheral blood: Predictive value for mortality in hemodialysis patients. Cytokine 2004, 27, 166-172. [CrossRef] [PubMed]
43. O'Rourke, R.W.; Kay, T.; Lyle, E.A.; Traxler, S.A.; Deveney, C.W.; Jobe, B.A.; Roberts, C.T., Jr.; Marks, D.; Rosenbaum, J.T. Alterations in peripheral blood lymphocyte cytokine expression in obesity. Clin. Exp. Immunol. 2006, 146, 39-46. [CrossRef] [PubMed]
44. Brockman, M.A.; Kwon, D.S.; Tighe, D.P.; Pavlik, D.F.; Rosato, P.C.; Sela, J.; Porichis, F.; Le Gall, S.; Waring, M.T.; Moss, K.; et al. IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells. Blood 2009, 114, 346-356. [CrossRef] [PubMed]
45. Stylianou, E.; Aukrust, P.; Kvale, D.; Muller, F.; Froland, S.S. IL-10 in HIV infection: Increasing serum IL-10 levels with disease progression-Down-regulatory effect of potent anti-retroviral therapy. Clin. Exp. Immunol. 1999, 116, 115-120. [CrossRef] [PubMed]
46. Clerici, M.; Wynn, T.A.; Berzofsky, J.A.; Blatt, S.P.; Hendrix, C.W.; Sher, A.; Coffman, R.L.; Shearer, G.M. Role of interleukin-10 in T helper cell dysfunction in asymptomatic individuals infected with the human immunodeficiency virus. J. Clin. Investig. 1994, 93, 768-775. [CrossRef] [PubMed]
47. Lee, S.; French, M.A.; Price, P. IL-23 and IFN-gamma deficiency in immunodeficient HIV patients who achieved a long-term increase in CD4 T-cell counts on highly active antiretroviral therapy. AIDS 2004, 18, 1337-1340. [CrossRef] [PubMed]
48. Hummelen, R.; Hemsworth, J.; Changalucha, J.; Butamanya, N.L.; Hekmat, S.; Habbema, J.D.; Reid, G. Effect of micronutrient and probiotic fortified yogurt on immune-function of anti-retroviral therapy naive HIV patients. Nutrients 2011, 3, 897-909. [CrossRef] [PubMed]
49. Buisson, S.; Benlahrech, A.; Gazzard, B.; Gotch, F.; Kelleher, P.; Patterson, S. Monocyte-derived dendritic cells from HIV type 1-infected individuals show reduced ability to stimulate T cells and have altered production of interleukin (IL)-12 and IL-10. J. Infect. Dis. 2009, 199, 1862-1871. [CrossRef] [PubMed]
50. Vanham, G.; Penne, L.; Fransen, K.; Kestens, L.; De Brabander, M. HIV-associated dysfunction of in vitro IL-12 production depends on the nature of the stimulus and on the CD4 T-cell count of the patient. Blood 2000, 95, 2185-2187. [PubMed]
51. Trinchieri, G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003, 3, 133-146. [CrossRef] [PubMed]
52. El Hed, A.; Khaitan, A.; Kozhaya, L.; Manel, N.; Daskalakis, D.; Borkowsky, W.; Valentine, F.; Littman, D.R.; Unutmaz, D. Susceptibility of human Th17 cells to human immunodeficiency virus and their perturbation during infection. J. Infect. Dis. 2010, 201, 843-854. [CrossRef] [PubMed]
53. Cunningham-Rundles, S.; Ahrne, S.; Johann-Liang, R.; Abuav, R.; Dunn-Navarra, A.M.; Grassey, C.; Bengmark, S.; Cervia, J.S. Effect of probiotic bacteria on microbial host defense, growth, and immune function in human immunodeficiency virus type-1 infection. Nutrients 2011, 3, 1042-1070. [PubMed]
54. O'Garra, A.; Murphy, K.M. From IL-10 to IL-12: How pathogens and their products stimulate APCs to induce T(H)1 development. Nat. Immunol. 2009, 10, 929-932. [CrossRef] [PubMed]
55. Van Hemert, S.; Meijerink, M.; Molenaar, D.; Bron, P.A.; de Vos, P.; Kleerebezem, M.;Wells, J.M.; Marco, M.L. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 2010, 10, 293. [CrossRef] [PubMed]
56. Amirayan-Chevillard, N.; Tissot-Dupont, H.; Capo, C.; Brunet, C.; Dignat-George, F.; Obadia, Y.; Gallais, H.; Mege, J.L. Impact of highly active anti-retroviral therapy (HAART) on cytokine production and monocyte subsets in HIV-infected patients. Clin. Exp. Immunol. 2000, 120, 107-112. [CrossRef] [PubMed]
57. Morris, S.C.; Orekhova, T.; Meadows, M.J.; Heidorn, S.M.; Yang, J.; Finkelman, F.D. IL-4 induces in vivo production of IFN-gamma by NK and NKT cells. J. Immunol. 2006, 176, 5299-5305. [CrossRef] [PubMed]
58. Leite-De-Moraes, M.C.; Hameg, A.; Pacilio, M.; Koezuka, Y.; Taniguchi, M.; Van Kaer, L.; Schneider, E.; Dy, M.; Herbelin, A. IL-18 enhances IL-4 production by ligand-activated NKT lymphocytes: A pro-Th2 effect of IL-18 exerted through NKT cells. J. Immunol. 2001, 166, 945-951. [CrossRef]
59. Hemsworth, J.C.; Hekmat, S.; Reid, G. Micronutrient supplemented probiotic yogurt for HIV-infected adults taking HAART in London, Canada. Gut Microbes 2012, 3, 414-419. [CrossRef] [PubMed]
60. Chandrasekhar, A.; Gupta, A. Nutrition and disease progression pre-highly active antiretroviral therapy (HAART) and post-HAART: Can good nutrition delay time to HAART and affect response to HAART? Am. J. Clin. Nutr. 2011, 94, 1703S-1715S. [CrossRef] [PubMed]
61. Odden, M.C.; Scherzer, R.; Bacchetti, P.; Szczech, L.A.; Sidney, S.; Grunfeld, C.; Shlipak, M.G. Cystatin C level as a marker of kidney function in human immunodeficiency virus infection: The FRAM study. Arch. Intern. Med. 2007, 167, 2213-2219. [CrossRef] [PubMed]
62. Ettinger, G.; MacDonald, K.; Reid, G.; Burton, J.P. The influence of the human microbiome and probiotics on cardiovascular health. Gut Microbes 2014, 5, 719-728. [CrossRef] [PubMed]