Generic placeholder image

Current HIV Research

Author(s): Sogol Jamshidi, Farah Bokharaei-Salim*, Javid Sadri Nahand, Seyed Hamidreza Monavari, Mohsen Moghoofei, Saba Garshasbi, Saeed Kalantari, Maryam Esghaei and Hamed Mirzaei

DOI: 10.2174/1570162X19666210906143136

DownloadDownload PDF Flyer Cite As
Evaluation of the Expression Pattern of 4 microRNAs and their Correlation with Cellular/viral Factors in PBMCs of Long Term Non-progressors and HIV Infected Naïve Individuals

Page: [42 - 53] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Background: Long-term non-progressors (LTNPs) are small subsets of HIV-infected subjects that can control HIV-1 replication for several years without receiving ART. The exact mechanism of HIV-1 suppression has not yet been completely elucidated. Although the modulatory role of microRNAs (miRNAs) in HIV-1 replication has been reported, their importance in LTNPs is unclear.

Objective: The aim of this cross-sectional study was to assess the expression pattern of miR-27b, -29, -150, and -221, as well as their relationship with CD4+ T-cell count, HIV-1 viral load, and nef gene expression in peripheral blood mononuclear cells (PBMCs) of untreated viremic patients and in LTNPs.

Methods: MiRNAs expression levels were evaluated with real-time PCR assay using RNA isolated from PBMCs of LTNPs, HIV-1 infected naive patients, and healthy people. Moreover, CD4 T-cell count, HIV viral load, and nef gene expression were assessed.

Results: The expression level of all miRNAs significantly decreased in the HIV-1 patient group compared to the control group, while the expression pattern of miRNAs in the LNTPs group was similar to that in the healthy subject group. In addition, there were significant correlations between some miRNA expression with viral load, CD4+ T-cell count, and nef gene expression.

Conclusion: The significant similarity and difference of the miRNA expression pattern between LNTPs and healthy individuals as well as between elite controllers and HIV-infected patients, respectively, showed that these miRNAs could be used as diagnostic biomarkers. Further, positive and negative correlations between miRNAs expression and viral/cellular factors could justify the role of these miRNAs in HIV-1 disease monitoring.

Keywords: Human immunodeficiency virus-1 (HIV-1), long-term non-progressors (LTNPs), peripheral blood mononuclear cells (PBMCs), viremic progressors (VPs), viremic controllers (VCs), elite controllers (ECs).

Graphical Abstract

[1]
Lang W, Perkins H, Anderson RE, Royce R, Jewell N, Winkelstein W Jr. Patterns of T lymphocyte changes with human immunodeficiency virus infection: from seroconversion to the development of AIDS. J Acquir Immune Defic Syndr 1989; 2(1): 63-9.
[PMID: 2783971]
[2]
Habeshaw JA, Dalgleish AG. The relevance of HIV env/CD4 interactions to the pathogenesis of acquired immune deficiency syndrome. J Acquir Immune Defic Syndr 1989; 2(5): 457-68.
[PMID: 2677311]
[3]
Maracy MR, Mostafaei S, Moghoofei M, Mansourian M. Impact of HIV risk factors on survival in Iranian HIV-infected patients: A Bayesian approach to retrospective cohort. HIV AIDS Rev 2017; 16(2): 100-6.
[http://dx.doi.org/10.5114/hivar.2017.68117]
[4]
Okulicz JF, Marconi VC, Landrum ML, et al. Clinical outcomes of elite controllers, viremic controllers, and long-term nonprogressors in the US Department of Defense HIV natural history study. J Infect Dis 2009; 200(11): 1714-23.
[http://dx.doi.org/10.1086/646609] [PMID: 19852669]
[5]
Dos Santos JS, de Almeida SM, Ferreira GS, et al. Host factor predictors in long-term nonprogressors HIV-1 infected with distinct viral clades. Curr HIV Res 2017; 15(6): 440-7.
[PMID: 29210660]
[6]
Zeller JM, McCain NL, Swanson B. Immunological and virological markers of HIV-disease progression. J Assoc Nurses AIDS Care: JANAC 1996; 7(1): 15-27.
[http://dx.doi.org/10.1016/S1055-3290(96)80034-3] [PMID: 8825177]
[7]
Merindol N, Berthoux L. Restriction factors in HIV-1 disease progression. Curr HIV Res 2015; 13(6): 448-61.
[http://dx.doi.org/10.2174/1570162X13666150608104412] [PMID: 26051387]
[8]
Cao Y, Qin L, Zhang L, Safrit J, Ho DD. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med 1995; 332(4): 201-8.
[http://dx.doi.org/10.1056/NEJM199501263320401] [PMID: 7808485]
[9]
Muñoz A, Kirby AJ, He YD, Margolick JB, Visscher B, Rinaldo C, et al. Long-term survivors with HIV-1 infection: incubation period and longitudinal patterns of CD4+ lymphocytes. J Acquired Immune Defici Syndro Human Retrovirolo: Official 1995; 8(5): 496-505.
[10]
Pantaleo G, Menzo S, Vaccarezza M, et al. Studies in subjects with long-term nonprogressive human immunodeficiency virus infection. N Engl J Med 1995; 332(4): 209-16.
[http://dx.doi.org/10.1056/NEJM199501263320402] [PMID: 7808486]
[11]
Sheppard HW, Lang W, Ascher MS, Vittinghoff E, Winkelstein W. The characterization of non-progressors: long-term HIV-1 infection with stable CD4+ T-cell levels. AIDS 1993; 7(9): 1159-66.
[http://dx.doi.org/10.1097/00002030-199309000-00002] [PMID: 8105806]
[12]
Madec Y, Boufassa F, Avettand-Fenoel V, et al. Early control of HIV-1 infection in long-term nonprogressors followed since diagnosis in the ANRS SEROCO/HEMOCO cohort. J Acquir Immune Defic Syndr 2009; 50(1): 19-26.
[http://dx.doi.org/10.1097/QAI.0b013e31818ce709] [PMID: 19295331]
[13]
Mikhail M, Wang B, Saksena NK. Mechanisms involved in non-progressive HIV disease. AIDS Rev 2003; 5(4): 230-44.
[PMID: 15012002]
[14]
Egaña-Gorroño L, Guardo AC, Bargalló ME, et al. MicroRNA profile in CD8+ T-lymphocytes from HIV-infected individuals: relationship with antiviral immune response and disease progression. PLoS One 2016; 11(5): e0155245.
[http://dx.doi.org/10.1371/journal.pone.0155245] [PMID: 27171002]
[15]
Walker BD. Elite control of HIV Infection: implications for vaccines and treatment. Topics in HIV Med 2007; 15(4): 134-6.
[16]
Reynoso R, Laufer N, Hackl M, et al. MicroRNAs differentially present in the plasma of HIV elite controllers reduce HIV infection in vitro. Sci Rep 2014; 4: 5915.
[http://dx.doi.org/10.1038/srep05915] [PMID: 25081906]
[17]
Okulicz JF, Lambotte O. Epidemiology and clinical characteristics of elite controllers. Curr Opin HIV AIDS 2011; 6(3): 163-8.
[http://dx.doi.org/10.1097/COH.0b013e328344f35e] [PMID: 21502920]
[18]
Martin-Gayo E, Yu XG. Dendritic cell immune responses in HIV-1 controllers. Curr HIV/AIDS Rep 2017; 14(1): 1-7.
[http://dx.doi.org/10.1007/s11904-017-0345-0] [PMID: 28110421]
[19]
Soliman M, Srikrishna G, Balagopal A. Mechanisms of HIV-1 control. Curr HIV/AIDS Rep 2017; 14(3): 101-9.
[http://dx.doi.org/10.1007/s11904-017-0357-9] [PMID: 28466391]
[20]
Gonzalo-Gil E, Ikediobi U, Sutton RE. Mechanisms of virologic control and clinical characteristics of HIV+ elite/viremic controllers. Yale J Biol Med 2017; 90(2): 245-59.
[PMID: 28656011]
[21]
Madec Y, Boufassa F, Porter K, Meyer L. collaboration C. Spontaneous control of viral load and CD4 cell count progression among HIV-1 seroconverters. AIDS 2005; 19(17): 2001-7.
[http://dx.doi.org/10.1097/01.aids.0000194134.28135.cd] [PMID: 16260907]
[22]
Lambotte O, Boufassa F, Madec Y, et al. HIV controllers: A homogeneous group of HIV-1-infected patients with spontaneous control of viral replication. Clin Infect Dis 2005; 41(7): 1053-6.
[http://dx.doi.org/10.1086/433188] [PMID: 16142675]
[23]
Grabar S, Selinger-Leneman H, Abgrall S, Pialoux G, Weiss L, Costagliola D. Prevalence and comparative characteristics of long-term nonprogressors and HIV controller patients in the French Hospital Database on HIV. AIDS 2009; 23(9): 1163-9.
[http://dx.doi.org/10.1097/QAD.0b013e32832b44c8] [PMID: 19444075]
[24]
Rausch JW, Le Grice SFJ. Characterizing the latent HIV-1 reservoir in patients with viremia suppressed on cART: progress, challenges, and opportunities. Curr HIV Res 2020; 18(2): 99-113.
[http://dx.doi.org/10.2174/1570162X18666191231105438] [PMID: 31889490]
[25]
Weiland M, Gao X-H, Zhou L, Mi Q-S. Small RNAs have a large impact: circulating microRNAs as biomarkers for human diseases. RNA Biol 2012; 9(6): 850-9.
[http://dx.doi.org/10.4161/rna.20378] [PMID: 22699556]
[26]
Zhao Y, Srivastava D. A developmental view of microRNA function. Trends Biochem Sci 2007; 32(4): 189-97.
[http://dx.doi.org/10.1016/j.tibs.2007.02.006] [PMID: 17350266]
[27]
Nahand JS, Taghizadeh-Boroujeni S, Karimzadeh M, et al. microRNAs: New prognostic, diagnostic, and therapeutic biomarkers in cervical cancer. J Cell Physiol 2019; 234(10): 17064-99.
[http://dx.doi.org/10.1002/jcp.28457] [PMID: 30891784]
[28]
Mendell JT. MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle 2005; 4(9): 1179-84.
[http://dx.doi.org/10.4161/cc.4.9.2032] [PMID: 16096373]
[29]
Ardekani AM, Naeini MM. The role of microRNAs in human diseases. Avicenna J Med Biotechnol 2010; 2(4): 161-79.
[PMID: 23407304]
[30]
Sullivan CS, Ganem D. MicroRNAs and viral infection. Mol Cell 2005; 20(1): 3-7.
[http://dx.doi.org/10.1016/j.molcel.2005.09.012] [PMID: 16209940]
[31]
Pauley KM, Cha S, Chan EK. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 2009; 32(3-4): 189-94.
[http://dx.doi.org/10.1016/j.jaut.2009.02.012] [PMID: 19303254]
[32]
Londin E, Loher P, Telonis AG, et al. Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. Proc Natl Acad Sci USA 2015; 112(10): E1106-15.
[http://dx.doi.org/10.1073/pnas.1420955112] [PMID: 25713380]
[33]
Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 2010; 101(10): 2087-92.
[http://dx.doi.org/10.1111/j.1349-7006.2010.01650.x] [PMID: 20624164]
[34]
Moghoofei M, Bokharaei-Salim F, Esghaei M, Keyvani H, Honardoost M, Mostafaei S, et al. microRNAs 29, 150, 155, 223 level and their relation to viral and immunological markers in HIV-1 infected naive patients. Future Virol 2018; 13(09): 637-45.
[http://dx.doi.org/10.2217/fvl-2018-0055]
[35]
Balasubramaniam M, Pandhare J, Dash C. Are microRNAs important players in HIV-1 infection? An update. Viruses 2018; 10(3): 110.
[http://dx.doi.org/10.3390/v10030110] [PMID: 29510515]
[36]
Swaminathan S, Zaunders J, Wilkinson J, Suzuki K, Kelleher AD. Does the presence of anti-HIV miRNAs in monocytes explain their resistance to HIV-1 infection? Blood 2009; 113(20): 5029-30.
[http://dx.doi.org/10.1182/blood-2009-01-196741] [PMID: 19443673]
[37]
Hariharan M, Scaria V, Pillai B, Brahmachari SK. Targets for human encoded microRNAs in HIV genes. Biochem Biophys Res Commun 2005; 337(4): 1214-8.
[http://dx.doi.org/10.1016/j.bbrc.2005.09.183] [PMID: 16236258]
[38]
Duan M, Yao H, Hu G, Chen X, Lund AK, Buch S. HIV Tat induces expression of ICAM-1 in HUVECs: implications for miR-221/-222 in HIV-associated cardiomyopathy. PLoS One 2013; 8(3): e60170.
[http://dx.doi.org/10.1371/journal.pone.0060170] [PMID: 23555914]
[39]
Adoro S, Cubillos-Ruiz JR, Chen X, et al. IL-21 induces antiviral microRNA-29 in CD4 T cells to limit HIV-1 infection. Nat Commun 2015; 6: 7562.
[http://dx.doi.org/10.1038/ncomms8562] [PMID: 26108174]
[40]
Monteleone K, Selvaggi C, Cacciotti G, et al. MicroRNA-29 family expression and its relation to antiviral immune response and viro-immunological markers in HIV-1-infected patients. BMC Infect Dis 2015; 15(1): 51.
[http://dx.doi.org/10.1186/s12879-015-0768-4] [PMID: 25808800]
[41]
Wang X, Ye L, Hou W, et al. Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood 2009; 113(3): 671-4.
[http://dx.doi.org/10.1182/blood-2008-09-175000] [PMID: 19015395]
[42]
Ma L, Shen C-J, Cohen EA, Xiong S-D, Wang J-H. miRNA-1236 inhibits HIV-1 infection of monocytes by repressing translation of cellular factor VprBP. PLoS One 2014; 9(6): e99535.
[http://dx.doi.org/10.1371/journal.pone.0099535] [PMID: 24932481]
[43]
Chiang K, Sung T-L, Rice AP. Regulation of cyclin T1 and HIV-1 Replication by microRNAs in resting CD4+ T lymphocytes. J Virol 2012; 86(6): 3244-52.
[http://dx.doi.org/10.1128/JVI.05065-11] [PMID: 22205749]
[44]
Ruiz-Mateos E, Ferrando-Martinez S, Machmach K, et al. High levels of CD57+CD28- T-cells, low T-cell proliferation and preferential expansion of terminally differentiated CD4+ T-cells in HIV-elite controllers. Curr HIV Res 2010; 8(6): 471-81.
[http://dx.doi.org/10.2174/157016210793499268] [PMID: 20636274]
[45]
Shacklett BL. Mucosal Immunity in HIV/SIV Infection: T Cells, B Cells and Beyond. Curr Immunol Rev 2019; 15(1): 63-75.
[http://dx.doi.org/10.2174/1573395514666180528081204] [PMID: 31327960]
[46]
Sun G, Li H, Wu X, et al. Interplay between HIV-1 infection and host microRNAs. Nucleic Acids Res 2012; 40(5): 2181-96.
[http://dx.doi.org/10.1093/nar/gkr961] [PMID: 22080513]
[47]
Ahluwalia JK, Khan SZ, Soni K, et al. Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology 2008; 5(1): 117.
[http://dx.doi.org/10.1186/1742-4690-5-117] [PMID: 19102781]
[48]
Rosa A, Chande A, Ziglio S, et al. HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation. Nature 2015; 526(7572): 212-7.
[http://dx.doi.org/10.1038/nature15399] [PMID: 26416734]
[49]
Mwimanzi P, Markle TJ, Martin E, et al. Attenuation of multiple Nef functions in HIV-1 elite controllers. Retrovirology 2013; 10(1): 1.
[http://dx.doi.org/10.1186/1742-4690-10-1] [PMID: 23289738]
[50]
Alsahafi N, Ding S, Richard J, et al. Nef proteins from HIV-1 elite controllers are inefficient at preventing antibody-dependent cellular cytotoxicity. J Virol 2015; 90(6): 2993-3002.
[http://dx.doi.org/10.1128/JVI.02973-15] [PMID: 26719277]
[51]
Buckheit RW III, Salgado M, Martins KO, Blankson JN. The implications of viral reservoirs on the elite control of HIV-1 infection. Cell Mol Life Sci 2013; 70(6): 1009-19.
[http://dx.doi.org/10.1007/s00018-012-1101-7] [PMID: 22864624]
[52]
Vahabpour R, Bokharaei-Salim F, Kalantari S, et al. HIV-1 genetic diversity and transmitted drug resistance frequency among Iranian treatment-naive, sexually infected individuals. Arch Virol 2017; 162(6): 1477-85.
[http://dx.doi.org/10.1007/s00705-017-3228-1] [PMID: 28181034]
[53]
Lodge R, Ferreira Barbosa JA, Lombard-Vadnais F, et al. Host microRNAs-221 and-222 inhibit HIV-1 entry in macrophages by targeting the CD4 viral receptor. Cell Rep 2017; 21(1): 141-53.
[http://dx.doi.org/10.1016/j.celrep.2017.09.030] [PMID: 28978468]
[54]
Munshi SU, Panda H, Holla P, Rewari BB, Jameel S. MicroRNA-150 is a potential biomarker of HIV/AIDS disease progression and therapy. PLoS One 2014; 9(5): e95920.
[http://dx.doi.org/10.1371/journal.pone.0095920] [PMID: 24828336]
[55]
Dubey RC, Alam NB, Gaur R. miR-150-mediated increase in glucose uptake in HIV-infected cells. J Med Virol 2020; 93(11): 6377-82.
[http://dx.doi.org/10.1002/jmv.26755] [PMID: 33368410]
[56]
Dehghani-Dehej F, Sarvari J, Esghaei M, et al. Presence of different hepatitis C virus genotypes in plasma and peripheral blood mononuclear cell samples of Iranian patients with HIV infection. J Med Virol 2018; 90(8): 1343-51.
[http://dx.doi.org/10.1002/jmv.24925] [PMID: 28845894]
[57]
Brooks DG, Hamer DH, Arlen PA, et al. Molecular characterization, reactivation, and depletion of latent HIV. Immunity 2003; 19(3): 413-23.
[http://dx.doi.org/10.1016/S1074-7613(03)00236-X] [PMID: 14499116]
[58]
Kiddle G, Hardinge P, Buttigieg N, et al. GMO detection using a bioluminescent real time reporter (BART) of loop mediated isothermal amplification (LAMP) suitable for field use. BMC Biotechnol 2012; 12(1): 15.
[http://dx.doi.org/10.1186/1472-6750-12-15] [PMID: 22546148]
[59]
Ntoumou E, Tzetis M, Braoudaki M, et al. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes. Clin Epigenetics 2017; 9(1): 127.
[http://dx.doi.org/10.1186/s13148-017-0428-1] [PMID: 29255496]
[60]
Keshavarz M, Dianat-Moghadam H, Sofiani VH, et al. miRNA-based strategy for modulation of influenza A virus infection. Epigenomics 2018; 10(6): 829-44.
[http://dx.doi.org/10.2217/epi-2017-0170] [PMID: 29888954]
[61]
Sadri Nahand J, Moghoofei M, Salmaninejad A, et al. Pathogenic role of exosomes and microRNAs in HPV-mediated inflammation and cervical cancer: A review. Int J Cancer 2020; 146(2): 305-20.
[http://dx.doi.org/10.1002/ijc.32688] [PMID: 31566705]
[62]
Gao L, Guo XK, Wang L, et al. MicroRNA 181 suppresses porcine reproductive and respiratory syndrome virus (PRRSV) infection by targeting PRRSV receptor CD163. J Virol 2013; 87(15): 8808-12.
[http://dx.doi.org/10.1128/JVI.00718-13] [PMID: 23740977]
[63]
Trobaugh DW, Gardner CL, Sun C, et al. RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 2014; 506(7487): 245-8.
[http://dx.doi.org/10.1038/nature12869] [PMID: 24352241]
[64]
Girardi E, López P, Pfeffer S. On the importance of host microRNAs during viral infection. Front Genet 2018; 9: 439.
[http://dx.doi.org/10.3389/fgene.2018.00439] [PMID: 30333857]
[65]
Taborda NA, Correa LA, Feria MG, Rugeles MT. The spontaneous control of hiv replication is characterized by decreased pathological changes in the gut-associated lymphoid tissue. Curr HIV Res 2018; 16(5): 338-44.
[http://dx.doi.org/10.2174/1570162X17666190130115113] [PMID: 30706820]
[66]
Wang B. Viral factors in non-progression. Front Immunol 2013; 4: 355.
[http://dx.doi.org/10.3389/fimmu.2013.00355] [PMID: 24400003]
[67]
Acheampong EA, Parveen Z, Muthoga LW, Kalayeh M, Mukhtar M, Pomerantz RJ. Human Immunodeficiency virus type 1 Nef potently induces apoptosis in primary human brain microvascular endothelial cells via the activation of caspases. J Virol 2005; 79(7): 4257-69.
[http://dx.doi.org/10.1128/JVI.79.7.4257-4269.2005] [PMID: 15767427]
[68]
Mak TW, Saunders ME. The immune response: basic and clinical principles. Academic Press 2005.
[69]
de Villiers M. Acquired immunodeficiency syndrome a forensic perspective. J Leg Med 2017; 37(3-4): 389-461.
[http://dx.doi.org/10.1080/01947648.2017.1385040] [PMID: 29473812]
[70]
Sadri Nahand J, Bokharaei-Salim F, Karimzadeh M, et al. MicroRNAs and exosomes: key players in HIV pathogenesis. HIV Med 2020; 21(4): 246-78.
[http://dx.doi.org/10.1111/hiv.12822] [PMID: 31756034]
[71]
Huang J, Wang F, Argyris E, et al. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med 2007; 13(10): 1241-7.
[http://dx.doi.org/10.1038/nm1639] [PMID: 17906637]
[72]
Poletti V, Mavilio F. Interactions between retroviruses and the host cell genome. Mol Ther Methods Clin Dev 2017; 8: 31-41.
[http://dx.doi.org/10.1016/j.omtm.2017.10.001] [PMID: 29159201]
[73]
V DU, De Crignis E, Re MC. Host restriction factors and human immunodeficiency virus (HIV-1): a dynamic interplay involving all phases of the viral life cycle. Curr HIV Res 2018; 16(3): 184-207.
[http://dx.doi.org/10.2174/1570162X16666180817115830] [PMID: 30117396]
[74]
Sharma N. Regulation of RNA polymerase II-mediated transcriptional elongation: Implications in human disease. IUBMB Life 2016; 68(9): 709-16.
[http://dx.doi.org/10.1002/iub.1538] [PMID: 27473825]
[75]
De Luca A, De Falco M, Baldi A, Paggi MG. Cyclin T: three forms for different roles in physiological and pathological functions. J Cell Physiol 2003; 194(2): 101-7.
[http://dx.doi.org/10.1002/jcp.10196] [PMID: 12494448]
[76]
De Luca A, Russo P, Severino A, et al. Pattern of expression of cyclin T1 in human tissues. J Histochem Cytochem 2001; 49(6): 685-92.
[http://dx.doi.org/10.1177/002215540104900602] [PMID: 11373315]
[77]
Moiola C, De Luca P, Gardner K, Vazquez E, De Siervi A. Cyclin T1 overexpression induces malignant transformation and tumor growth. Cell Cycle 2010; 9(15): 3119-26.
[http://dx.doi.org/10.4161/cc.9.15.12526] [PMID: 20714219]
[78]
Das B, Dobrowolski C, Shahir A-M, et al. Short chain fatty acids potently induce latent HIV-1 in T-cells by activating P-TEFb and multiple histone modifications. Virology 2015; 474: 65-81.
[http://dx.doi.org/10.1016/j.virol.2014.10.033] [PMID: 25463605]
[79]
Witwer KW, Watson AK, Blankson JN, Clements JE. Relationships of PBMC microRNA expression, plasma viral load, and CD4+ T-cell count in HIV-1-infected elite suppressors and viremic patients. Retrovirology 2012; 9(1): 5.
[http://dx.doi.org/10.1186/1742-4690-9-5] [PMID: 22240256]
[80]
Egaña-Gorroño L, Escribà T, Boulanger N, et al. Differential microRNA expression profile between stimulated PBMCs from HIV-1 infected elite controllers and viremic progressors. PLoS One 2014; 9(9): e106360.
[http://dx.doi.org/10.1371/journal.pone.0106360] [PMID: 25225963]
[81]
Yousefpouran S, Mostafaei S, Manesh PV, et al. The assessment of selected MiRNAs profile in HIV, HBV, HCV, HIV/HCV, HIV/HBV Co-infection and elite controllers for determination of biomarker. Microb Pathog 2020; 147: 104355.
[http://dx.doi.org/10.1016/j.micpath.2020.104355] [PMID: 32569788]
[82]
Misiewicz-Krzeminska I, Krzeminski P, Corchete LA, et al. Factors regulating microRNA expression and function in multiple myeloma. Noncoding RNA 2019; 5(1): 9.
[http://dx.doi.org/10.3390/ncrna5010009] [PMID: 30654527]
[83]
Leung AK, Sharp PA. MicroRNA functions in stress responses. Mol Cell 2010; 40(2): 205-15.
[http://dx.doi.org/10.1016/j.molcel.2010.09.027] [PMID: 20965416]
[84]
Nguyen TH, Liu X, Su ZZ, Hsu AC-Y, Foster PS, Yang M. Potential role of MicroRNAs in the regulation of antiviral responses to influenza infection. Front Immunol 2018; 9: 1541.
[http://dx.doi.org/10.3389/fimmu.2018.01541] [PMID: 30022983]
[85]
Gupta P, Liu B, Wu JQ, et al. Genome-wide mRNA and miRNA analysis of peripheral blood mononuclear cells (PBMC) reveals different miRNAs regulating HIV/HCV co-infection. Virology 2014; 450-451: 336-49.
[http://dx.doi.org/10.1016/j.virol.2013.12.026] [PMID: 24503097]
[86]
Murray DD, Suzuki K, Law M, et al. Circulating miR-122 and miR-200a as biomarkers for fatal liver disease in ART-treated, HIV-1-infected individuals. Sci Rep 2017; 7(1): 10934.
[http://dx.doi.org/10.1038/s41598-017-11405-8] [PMID: 28883647]
[87]
Mayeux R. Biomarkers: potential uses and limitations. NeuroRx 2004; 1(2): 182-8.
[http://dx.doi.org/10.1602/neurorx.1.2.182] [PMID: 15717018]
[88]
Silva SS, Lopes C, Teixeira AL, Carneiro de Sousa MJ, Medeiros R. Forensic miRNA: potential biomarker for body fluids? Forensic Sci Int Genet 2015; 14: 1-10.
[http://dx.doi.org/10.1016/j.fsigen.2014.09.002] [PMID: 25280377]
[89]
Roser AE, Caldi Gomes L, Schünemann J, Maass F, Lingor P. Circulating miRNAs as diagnostic biomarkers for Parkinson’s disease. Front Neurosci 2018; 12: 625.
[http://dx.doi.org/10.3389/fnins.2018.00625] [PMID: 30233304]
[90]
Rome S. Use of miRNAs in biofluids as biomarkers in dietary and lifestyle intervention studies. Genes Nutr 2015; 10(5): 483.
[http://dx.doi.org/10.1007/s12263-015-0483-1] [PMID: 26233309]
[91]
Rosca A, Anton G, Botezatu A, et al. miR-29a associates with viro-immunological markers of HIV infection in treatment experienced patients. J Med Virol 2016; 88(12): 2132-7.
[http://dx.doi.org/10.1002/jmv.24586] [PMID: 27232693]