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Antiretroviral remedy inhibits matrix metalloproteinase-9 from blood mononuclear cells of HIV-contaminated sufferers

Introduction

HIV infection is frequently linked to loads of neurological diseases, the most severe being HIV-linked dementia (HAD). The pathogenetic mechanisms of blood–mind barrier disruption and demyelination, which represent the leading characteristics of HAD, are yet to be described. recent reviews have advised that the development of neurological syndromes in HAD might be a result of adjustments within the blood–mind barrier that cause an improved migration of leukocytes into the important nervous device (CNS) [1]. The entry of leukocytes into the CNS is dependent in a couple of factors including the expression of matrix metalloproteinases (MMP). Likewise, HIV-wonderful leukocytes transmigrate during the endothelial basement membranes when getting into the spleen and/or lymph nodes in a manner that also requires MMP.

The MMP form a large family of zinc-containing endopeptidases that degrade extracellular matrix and basement membrane compounds (collagens, gelatine, laminin, fibronectin). They share ordinary structured domains however fluctuate with respect to their cellular sources, inducibility and effectivity of substrate utilization.

The endeavor of MMP is particularly regulated each on the stage of gene expression and through activation of latent pro-MMP to lively enzymes [2]. within the extracellular milieu, the pastime of these enzymes is managed by means of 4 natural tissue inhibitors of matrix metalloproteinases (TIMP). changes within the first-rate stability between MMP and their tissue inhibitors drives extracellular matrix turnover and may be important to irritation in infection in addition to other pathological condition, including neurotoxicity.

both cells of the myeloid lineage and lymphocytes produce MMP and MMP are concerned in many physiological hobbies, together with standard tissue remodelling and wound restoration, as well as in lots of pathological procedures such as tumour increase and metastasis, rheumatoid arthritis and assorted sclerosis [3]. recent findings imply that MMP play a vital role in the pathophysiology of tissue harm and dysfunction all through HIV infection, leading to dysregulation of T phone and monocyte/macrophage invasiveness. certainly, in-vitro studies have proven that HIV-1 infection increases T mobilephone and monocyte secretion of gelatinease B (MMP-9) as well as their means to traverse artificial basement membrane limitations. this means a important position for MMP-9 in migration and spreading of HIV-infected mononuclear cells into tissues and due to this fact within the evolution of HIV an infection [4–6]. targeting MMP enzyme endeavor, hence, may constitute a novel therapeutical approach for HAD and other HIV-associated pathologies [7].

The introduction of amazing antiretroviral remedy (art) has dramatically changed the evolution of HIV infection, leading to a reduction in the occurrence of neurological disorders. we've in the past established that two antiretroviral medication, zidovudine (AZT) and indinavir, inhibit gelatinease A (MMP-2) and MMP-9 expression in glial cells. This discovering means that the really helpful effect of art observed in HIV-infected sufferers could be, at the least partially, ascribed to the discount of MMP secretion and/or expression from glial cells [8].

given that no in-vivo facts are currently available on the putative extended levels of MMP-9 in peripheral blood mononuclear cells (PBMC) of HIV-infected sufferers, the existing examine investigated no matter if or no longer paintings influences the free up of MMP-9 in the PBMC of such patients.

materials and techniques Reagents

RPMI, fetal bovine serum, penicillin and streptomycin have been purchased from GIBCO (Paisley, Scotland); gelatine, fluorescein isothiocyanate (FITC), bovine serum albumin and Trypan blue from Sigma (St Louis, Missouri, united states); polystyrene microspheres from Polysciences (Warrington, Pennsylvania, u . s .); PD-10 columns from Pharmacia (Uppsala, Sweden) and typical proteins and R-250 Coomassie stunning blue from Bio-Rad (Hercules, California, us of a). Primer pairs certain for MMP-2, MMP-9 and glyceraldehyde-three-phosphate dehydrogenase (GAPDH) were from Sigma Genosys (Cambridge, UK). RNeasy mini package become from Qiagen (Valencia, California, united states). the entire reagents for reverse transcriptase polymerase chain reaction (RT-PCR) had been bought from Invitrogen (San Diego, California, country). Purified MMP-2 and MMP-9 have been bought from Alexis Biochemicals (San Diego, California, country). because the MMP-9 become purified from human neutrophil granulocytes, it additionally contained covalent MMP-9–NGAL advanced.

patients

a complete of forty six HIV-infected patients (32 men and 14 adult females (median age, 39 years; range, 26–sixty six) from the branch of Infectious and Tropical illnesses of ‘La Sapienza’ university of Rome have been covered in this study. HIV seropositivity turned into determined via enzyme-linked immunosorbent assay and demonstrated by Western blot analysis (Chiron, Emeryville California, u . s . a .) based on the company's instructions. among the HIV-infected patients, 30 have been receiving artwork (median CD4 mobilephone count number, 268 cells/μl; median CD4/CD8, 0.29; median HIV-RNA, 21 111 copies/ml), whereas 16 sufferers with advanced an infection were naive for any paintings medication (median CD4 phone count number, 126 cells/μl; median CD4/CD8, 0.17; median HIV-RNA, a hundred ninety 833 copies/ml). All sufferers have been handled with two nucleoside reverse-transcriptase inhibitors (NRTI) and one or two protease inhibitors (PI). Seventeen adult match donors (HD) have been covered as HIV-poor controls. All subjects gave suggested consent for the study.

HIV RNA stages and T telephone counts

Plasma HIV-1–RNA degrees were measured the usage of quantitative RT-PCR (Amplicor HIV display screen; Roche Diagnostic methods, Branchburg, New Jersey, country). The limit of detection become 50 copies/ml. CD4 and CD8 lymphocyte numbers have been assessed in blood amassed in ethylenediaminetetracetic acid (EDTA)-containing tubes. Two-coloration flow cytometric evaluation changed into performed with the Becton Dickinson flow cytometer FACScan using the total-blood lysis process and SimulTEST reagents (Becton Dickinson, San Jose, California, usa).

Specimen assortment and cellphone isolation

Venous blood samples have been accrued into EDTA-containing tubes and plasma samples and cells were separated immediately. PBMC had been isolated from peripheral blood using a Ficoll–Hypaque gradient. After isolation, the cells were washed, counted and suspended in RPMI 1640 containing 10% autologous serum at a awareness of 4 × 106 cells/ml. Samples of PBMC suspension (100 μl, four × 105 cells/neatly) had been plated in 24-smartly microtitre plates in serum-free medium and cultured at 37°C in 5% CO2. After incubation for twenty-four h, the culture medium became accumulated, centrifuged at 10 000 g and supernatants were assayed for MMP-2 and MMP-9. Cells have been subjected to complete RNA extraction for subsequent determination of gene expression by using RT-PCR.

Detection of MMP-9 activity with the aid of zymography

Gelatinases in mobilephone lifestyle supernatants had been detected by sodium dodecyl sulphate (SDS)–polyacrylamide gel electrophoresis in line with a amendment of the method of Heussen and Dowdle [9], as already described by means of Liuzzi et al. [8]. in brief, every 50 μl sample of supernatant become supplemented with 30 μl electrophoresis loading buffer containing SDS. The samples have been then separated in a 7.5% polyacrylamide gel that had been copolymerized with 0.1% (w/v) gelatine. Stacking gel contained 5.four% polyacrylamide. Electrophoresis was performed at 4°C for about 18 h at 70 V. To get rid of SDS and reactivate the enzyme after electrophoresis, the gels have been washed twice for 20 min in 2.5% (w/v) Triton X-one hundred in 50 mmol/l Tris-HCl, 10 mmol/l CaCl2, pH 7.four after which incubated in 1% (w/v) Triton X-a hundred in 50 mmol/l Tris-HCl, 10 mmol/l CaCl2, pH 7.4.

Gelatinase activity turned into detected as a white band on a blue history on gels stained with Coomassie staggering blue R-250. MMP-9 recreation was quantified by means of scanning densitometry and computerized photograph evaluation (photograph grasp identity application, Pharmacia, Biotech, Uppsala, Sweden) and expressed as absorbance × mm2, representing the scanning area beneath the curves, which takes into consideration both brightness and width of the substrate lysis zone.

Detection of the net undertaking of MMP-9 by way of move cytometric assay

MMP-9 net undertaking in telephone culture supernatants turned into determined by using a fluorescent activated substrate conversion assay (FASC) according to the digestion of FITC-conjugated gelatine immobilized on microspheres and stream cytometric assay according to the formula of St-Pierre et al. [10].

in brief, 300 μl gelatine, dissolved in carbonate buffer (pH 9.2) to a last attention of two mg/ml was incubated for 24 h at 4°C with 10 μl of FITC dissolved in dimethyl sulphoxide. Free FITC molecules were removed by means of chromatography on PD-10 columns. Polystyrene microspheres 15.5 μm in diameter were incubated for two h at 37°C with FITC-conjugated gelatine (1 mg/ml in phosphate-buffered saline, pH 7,4) to permit non covalent adsorption. After two washes in phosphate buffer containing 0.5% bovine serum albumin and zero.05% sodium azide (PBA), the microspheres were kept at 4°C in PBA (106 beads/ml) in the dark before use.

The enzymatic response became conducted in a closing volume of 100 μl the use of serum-free RPMI as response buffer; 50 μl telephone supernatant turned into incubated with 10 μl FITC–gelatine-coated microspheres at 37°C for 18 h. The enzymatic response changed into stopped by way of adding 1 ml PBA, adopted by means of two washes of the microspheres. The sedimented beads were then resuspended in 0.5 ml PBA and analysed via FACScan with general optics for the detection of FITC fluorescence. Microsphere fluorescence turned into measured on a single-parameter histogram on a wide range. Between one thousand and 5000 movements were analysed for each histogram. The net activity of MMP-9 turned into calculated as the lower in fluorescence detected in each pattern in assessment with a terrible handle, represented via FITC–gelatine-lined microspheres incubated in serum-free RPMI. For each and every assay, the MMP-9 web exercise became quantified the use of a standard curve constructed the usage of commonplace quantities of MMP-9 usual.

RNA analysis

total cellular RNA turned into isolated from PBMC the usage of an RNeasy mini kit based on the company's instructions. RNA changed into precipitated with ethanol, resuspended in RNase-free water and its quantity and great changed into decided spectrophotometrically at 260/280 nm. RNA samples were kept at −70°C. Complementary DNA (cDNA) become prepared by using reverse transcription using random primers. The cDNA became used to make bigger a 517 bp fragment using selected primers (feel 5′-AGGCAGCTGGCAGAGGAATAC-3′; antisense 5′-TGCCCAGGGACCACAACT-3′) for the human MMP-9 sequence. After preliminary experiments to check the most efficient PCR biking conditions, 25 cycles of PCR were performed every including denaturation at ninety four°C for 45 sec, annealing at fifty nine°C for 1 min and extension at seventy two°C for 1 min in a thermal cycler (PTC-a hundred Programmable Thermac Controller, MJ research, Walthan, Massachusetts, united states of america). PCR products have been separated electrophoretically on 1.5% agarose gels and visualized by way of ethidium bromide staining. Gels were then processed for densitometric analysis as described above for protein gels. normal molecular dimension markers, bad manage (PCR combine with out sample cDNA) and positive controls had been run with every PCR assay. Amplification of a 308 bp fragment of human GAPDH (feel 5′-CTTCACCACCATGGAGAAGGC-3′; antisense 5′-GGCATGGGACTGTGGTCATGAG-three′), a comparatively invariant inside reference RNA, became carried out in parallel, and cDNA quantities had been standardized to equivalent GAPDH mRNA ranges. The primer units notably diagnosed only the genes of activity as indicated with the aid of amplification of a single band of the anticipated measurement of the PCR products.

Statistical evaluation

Parametric one-manner evaluation of variance, ANOVA, or the non-parametric Kruskall–Wallis verify were used to examine the three agencies, as applicable. In instances of statistical value, Tukey look at various or Dunn's assorted comparison submit-verify had been used for the pair-intelligent evaluation of groups. The correlation between MMP-9 activity and HIV viral load turned into carried out the use of the Spearman rank order correlation examine.

reported P values had been considered statistically giant at P < 0.05. facts have been analysed by using the statistical software SigmaStat for windows (version 3.0. SPSS, Chicago, Illinois, usa).

results The impact of antiretroviral remedy on the extended MMP-9 tiers in HIV-positive sufferers

In PBMC supernatants analysed by using zymography, MMP-9 turned into observed in all samples however at different ranges, whereas handiest traces of MMP-2 were detected in both HIV-infected subjects and HD without enormous variations (Fig. 1a).

tiers of MMP-9 had been tremendously multiplied in 24 h subculture supernatants from PBMC of HIV-wonderful, art-naive patients (suggest, 36.7; SD, 6.0) in assessment with HIV-negative controls (mean, 23.0; SD, 6.three). against this, within the artwork-handled patients, MMP-9 tiers had been tremendously lessen (suggest, 23.eight; SD, 7.5) than those measured in the untreated HIV-contaminated people (Fig. 1b).

MMP-9 gene expression in HIV-effective patients

To investigate whether the lowered MMP-9 production in PBMC of artwork-treated patients resulted from inhibition of mRNA transcription, RT-PCR evaluation of MMP-9 mRNA expression changed into performed after normalization with GAPDH mRNA, a housekeeping gene product used as internal control (Fig. 2). The expression of MMP-9 was greatly expanded in artwork-naive individuals (suggest, eight.7; SD, 1.1; P < 0.05) in comparison with HD (imply, 5.four; SD, 1.7). against this, paintings-treated topics showed a major inhibition of MMP-9 (suggest, four.1; SD, 1.6; P < 0.05) in assessment with art-naive subjects. No colossal changes had been present in the mRNA expression of MMP-9 between HD and paintings-treated sufferers.

Detection of MMP-9 net undertaking in subculture supernatants from peripheral mononuclear cells

The useful endeavor of MMP-9 in telephone supernatants changed into detected by using a FASC assay [9]. As illustrated through the sharp reduce of imply fluorescence depth (MIF), a high degree of MMP-9 purposeful recreation become present in PBMC supernatants of the art-naive patients. No tremendous decrease of MIF was accompanied when FITC–gelatine-lined microspheres have been incubated with PBMC supernatants from each HD and paintings-treated topics (Fig. 3a).

As shown in Fig. 3b, the suggest percentage of MIF in art-naive subjects changed into tremendously lowered (65%) compared with that followed in HD (sixteen%) and art-handled subjects (20%).

The amount of purposeful activity of MMP-9 become further quantified in all samples and for each assay, the usage of a standard curve developed with universal quantities of MMP-9 standard (Fig. 4). huge tiers of free lively MMP-9 have been found simplest in PBMC supernatants from art-naive sufferers (mean, 104.0 ng; SD, 2.6; range, ninety three–one zero five), however not in supernatants from artwork-handled people (imply, 2.2 ng; SD, 0.5; latitude, 1.eight–2.5) nor in HD (suggest, 2.0 ng; SD, 0.5; range, 1.4–2.6) (Fig. 5).

Fig. 4

Fig. four

Fig. 5

Fig. 5

MMP-9 exercise is not correlated to viral load

with the intention to study no matter if the elevation of MMP-9 and the downregulation with the aid of therapy could be correlated with HIV viral load, the connection between MMP-9 activity and plasma HIV-1 RNA ranges was calculated in each art-naive and artwork-handled patients. No significant correlation become found between HIV viral load and MMP-9 recreation in both art-naive (r = 0.262; P = 0.339) and art-treated individuals (r = -0.336; P = 0.0797).

dialogue

in the era of potent art, HAD nonetheless represents an important explanation for morbidity and mortality in patients with HIV an infection. Pathological evidence suggests that HAD might also happen resulting from an alteration of the blood–mind barrier. one more talents link to AIDS pathology is the discovering of HIV reservoirs in the lymphoid organs, including spleen, lymph nodes and mucosa-linked lymphoid tissues. elevated blood–mind barrier permeability may contribute to the building of dementia by means of facilitating the entry of activated and infected mononuclear cells, in addition to toxic serum proteins, into the CNS. One mechanism during which blood–mind barrier permeability may be altered is through multiplied activity of selected MMP.

Viral infection of host cells has been proven to set off the expression of MMP, in specific MMP-9 [11]. similarly, in-vitro reports point out that HIV-1 infection of T cells and monocytes ends up in extended secretion of extracellular degrading MMP and enhances the means of these cells to traverse the basement membrane [5]. It has been shown that the HIV viral proteins Tat and gp120 can upregulate MMP-9 secretion from monocytes and T cells [12,13]. in addition, the intracisternal injection of the HIV Nef protein in an experimental rat model of HIV brought about a disruption of the blood–mind barrier that correlated with the changes in cerebrospinal fluid MMP-9 tiers [14]. in addition, pretreatment with an MMP inhibitor abrogated the accelerated vascular permeability.

There aren't any ex-vivo information bearing on the construction of MMP from mononuclear cells of HIV-1-contaminated individuals or on the impact of paintings on MMP and TIMP liberate. in the existing look at, they verified that PBMC from HIV-contaminated sufferers secrete multiplied tiers of MMP-9 compared with HD. This finding highlights the contribution of MMP within the pathogenesis of HAD. combating inflammatory cells from infiltrating the CNS may additionally, therefore, symbolize a reasonable therapeutic approach to handle HIV-related neurological ailments.

in this context, it's price bringing up their contemporary demonstration that zidovudine and indinavir inhibit the in-vitro expression of MMP-2 and MMP-9 in glial cells [8].

here they now have investigated the effect of art on MMP-9 production from PBMC remoted from HIV-contaminated sufferers and have supplied the primary experimental demonstration that art greatly downregulates the expression of MMP-9 in naturally contaminated PBMC.

beneath physiological situations, MMP pastime is the effect of a cautious balance between two tactics: activation of proenzymes and inhibition through selected tissue inhibitors of MMP, the TIMPs, which form good, non-covalent enzyme-inhibitor complexes with active MMP. for this reason, matrix degradation ultimately depends upon the ratio of free energetic gelatinase to TIMP-complexed types. because zymography exhibits latent and lively sorts of gelatinases and dissociates the MMP–TIMP complexes, it can't be used to measure the internet activity displayed in phone supernatants in presence of TIMP. as a way to complement their zymography information, they measured the practical activity of MMP-9 in PBMC supernatants using the FASC assay [10]. This formula permits measurement of the internet exercise of MMP-9 due to the stability between MMP-9 and its inhibitor TIMP-1 with the aid of monitoring the reduce of the fluorescence emitted by a FITC-conjugated substrate immobilized on polystyrene microspheres in the presence of the enzyme. using this technique, they naturally validated that only samples from artwork-naive individuals displayed MMP-9 useful recreation; samples from paintings-handled topics had little or no free lively MMP-9, which turned into akin to the condition accompanied for HD samples. This shows that in HIV-contaminated individuals subjected to artwork, MMP-9 levels are lower than in untreated patients and moreover counterbalanced with the aid of absence of activation or inhibition. even if this steadiness is only through MMP-9 legislation or additionally reflects an effect of art on TIMP-1 continues to be to be centered.

there's little tips on the legislation of the matrix-degrading enzymes within the brain tissue microenvironment with the aid of their TIMP inhibitors. Activated brain mononuclear phagocytes can also contribute to the excess MMP activity inside the brain, both through directly secreting MMP or cutting back secretion of the TIMP that counteracts the MMP [15]. it is noteworthy that improved MMP-9 and decreased TIMP-1 have been observed within the cerebrospinal fluid of patients with HAD [16,17], implying that the balance between proteases and their inhibitors has critical organic consequences.

using RT-PCR, they confirmed that TIMP-1 expression is not likely to be regulated in PBMC from HIV-contaminated sufferers whether or not handled by using artwork (statistics now not shown). certainly, MMP-9 expression become not most effective found to be accelerated in art-naive subjects but changed into additionally inhibited through paintings.

The mechanisms worried in MMP-9 modulation all through the path of HIV infection don't seem to be well centered. It has been lately validated that the in-vitro treatment of simple T cells with the viral protein gp120 prompts MMP-9 transcription by way of the p38 and SAPK/JNK MAPK pathways, and that inhibition of p38 MAPK activation abolished MMP-9 expression [13], indicating an instantaneous impact of HIV on MMP-9 expression. In their experiments, they didn't find any correlation between viral load and MMP-9 endeavor in either artwork-naive or artwork-handled patients. a couple of reviews point out that antiretroviral medication, principally HIV protease inhibitors, exert certain results on cellular turnover, apoptosis and proteolytic programs that are unbiased from their ability to dam HIV replication [18,19]. In a contemporary analyze, Lichtner and coworkers showed that the potential of HIV protease inhibitors to reverse phone apoptosis in each infected and uninfected cells is end result of the their direct inhibition of cysteine proteases, as calpains [20]. On the foundation of these observations, antiretroviral medicine might exert a direct effect on MMP unencumber, regardless of their endeavor on viral replication. then again, in a previous examine the usage of an in-vitro assay, they proven that the antiretroviral medicine zidovudine and indinavir did not directly inhibit the exercise of MMP-2 and MMP-9 [8].

hence, they can't exclude the probability that art may additionally modulate MMP unencumber by means of indirect mechanisms. certainly, the elevated production of MMP in patients with AIDS may be ascribed to the state of exaggerated immune activation seen all the way through the direction of HIV an infection [21]. This activation might, in flip, result in upregulation of proinflammatory cytokines dependable of MMP-9 overexpression. during this appreciate, it has been recently tested that soluble HIV Tat upregulates MMP-9 expression in monocytes through inducing the creation of tumour necrosis factor α and interleukin 1β [22]. some of the main immunologic outcomes of paintings is the discount of this state of immune activation, which is intently involving the degree of viral suppression and immune reconstitution. in this respect, art could inhibit the MMP unencumber by using reducing the HIV-linked immune activation.

In conclusion, the current findings display for the primary time that art can reduce the skill of PBMC from HIV-infected sufferers to secrete expanded amounts of MMP-9. This provides a novel perception into the modulatory results of antiretroviral drugs on MMP that may well be independent from their means to block HIV replication. The figuring out of the molecular mechanisms of MMP-9 activation in HIV-infected sufferers and its downregulation via art may additionally give new scientific perspectives helpful to mitigate the MMP-linked damage all over HIV infection.

Acknowledgements

The authors prolong a unique because of Dr Guglielmina Chimienti for the statistical analysis of records.

References 1. Persidsky Y, Zheng J, Miller D, Gendelman HE. Mononuclear phagocytes mediate blood–brain barrier compromise and neuronal harm all over HIV-1-linked dementia. J Leukoc Biol 2000; 68:413–422. 2. Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G. Biochemistry and molecular biology of gelatinease B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002; 37:375–536. three. Malemud CJ. Matrix metalloproteinases (MMPs) in health and disease: a top level view. entrance Biosci 2006; 11:1696–1701. 4. Weeks BS. The function of HIV-1 activated leukocyte adhesion mechanisms and matrix metalloproteinase secretion in AIDS pathogenesis. Int J Mol Med 1998; 1:361–366. 5. Dhawan S, Weeks BS, Soderland C, Schnaper HW, Toro LA, Asthana SP, et al. HIV-1 an infection alters monocyte interactions with human microvascular endothelial cells. J Immunol 1995; 154:422–432. 6. Chapel C, Camara V, Clayette P, Salvat S, Mabondzo A, Leblond V, et al. Modulations of ninety two kDa gelatinease B and its inhibitors are associated with HIV-1 infection in human macrophage cultures. Biochem Biophys Res Commun 1994; 204:1272–1278. 7. Webster NL, Crowe SM. Matrix metalloproteinases, their construction by using monocytes and macrophages, and their abilities position in HIV-linked diseases. J Leukoc Biol 2006; eighty:1–15. 8. Liuzzi GM, Mastroianni CM, Latronico T, Mengoni F, Fasano A, Lichtner M, et al. Anti-HIV medication lessen the expression of matrix metalloproteinases in astrocytes and microglia. mind 2004; 127:398–407. 9. Heussen C, Dowdle EB. Electrophoretic evaluation of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal Biochem 1980; 102:196–202. 10. St-Pierre Y, Desrosiers M, Tremblay P, Esteve PO, Opdenakker G. circulate cytometric evaluation of gelatinease B (MMP-9) recreation the use of immobilized fluorescent substrate on microspheres. Cytometry 1996; 25:374–380. 11. Ghorpade A, Persidskaia R, Suryadevara R, Che M, Liu XJ, Persidsky Y, et al. Mononuclear phagocyte differentiation, activation, and viral infection alter matrix metalloproteinase expression: implications for human immunodeficiency virus type 1-associated dementia. J Virol 2001; seventy five:6572–6583. 12. Lafrenie RM, Wahl LM, Epstein JS, Hewlett IK, Yamada KM, Dhawan S. HIV-1-Tat modulates the characteristic of monocytes and alters their interactions with microvessel endothelial cells. A mechanism of HIV pathogenesis. J Immunol 1996; 156:1638–1645. 13. Misse D, Esteve PO, Renneboog B, Vidal M, Cerutti M, St Pierre Y, et al. HIV-1 glycoprotein 120 induces the MMP-9 cytopathogenic aspect creation that is abolished by using inhibition of the p38 mitogen-activated protein kinase signaling pathway. Blood 2001; 98:541–547. 14. Sporer B, Koedel U, Paul R, Kohleisen B, Erfle V, Fontana A, et al. Human immunodeficiency virus type-1 Nef protein induces blood-mind barrier disruption within the rat: role of matrix metalloproteinase-9. J Neuroimmunol 2000; 102:one hundred twenty five–130. 15. Elkington PTG, O'Kane CM, Friedland JS. The paradox of matrix metalloproteinases in infectious disease. Clin Exp Immunol 2005; 142:12–20. 16. Liuzzi GM, Mastroianni CM, Santacroce MP, Fanelli M, D'Agostino C, Vullo V, et al. multiplied pastime of matrix metalloproteinases in the cerebrospinal fluid of sufferers with HIVassociated neurological illnesses. J Neurovirol 2000; 6:156–163. 17. Suryadevara R, Holter S, Borgmann ok, Persidsky R, Labenz-Zink C, Persidsky Y, et al. law of tissue inhibitor of metalloproteinase-1 by using astrocytes: hyperlinks to HIV-1 dementia. Glia 2003; forty four:47–56. 18. Badley ad. In vitro and in vivo outcomes of HIV protease inhibitors on apoptosis. phone dying range 2005; 12(Suppl 1):924–931. 19. Ghibelli L, Mengoni F, Lichtner M, Coppola S, de Nicola M, Bergamaschi A, et al. Anti-apoptotic impact of HIV protease inhibitors via direct inhibition of calpain. Biochem Pharmacol 2003; 66:1505–1512. 20. Lichtner M, Mengoni F, Mastroianni CM, Sauzullo I, Rossi R, De Nicola M, et al. HIV protease inhibitor therapy reverses neutrophil apoptosis in AIDS patients with the aid of direct calpain inhibition. Apoptosis 2006; eleven:781–787. 21. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, Lange JM, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17:1881–1888. 22. Lafrenie RM, Wahl LM, Epstein JS, Yamada KM, Dhawan S. Activation of monocytes by way of HIV-Tat treatment is mediated with the aid of cytokine expression. J Immunol 1997; 159:4077–4083. keyword phrases:

matrix metalloproteinases; TIMP-1; antiretroviral therapy; HIV-linked dementia; peripheral blood mononuclear cells

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