SpringerLink
Log in

PBMC MicroRNAs: Promising Biomarkers for the Differential Diagnosis of COVID-19 Patients with Abnormal Coagulation Indices

  • Original Paper
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

MicroRNAs, or miRNAs, may involve in coagulation and inflammation pathways caused by severe Coronavirus disease (COVID-19). Accordingly, this attempt was made to explore the behavior of peripheral blood mononuclear cells (PBMCs) miRNAs as effective biomarkers to diagnose COVID-19 patients with normal and abnormal coagulation indices. We selected the targeted miRNAs (miR-19a-3p, miR-223-3p, miR-143-5p, miR-494-3p and miR-301a-5p) according to previous reports, whose PBMC levels were then determined by real-time PCR. Receiver operating characteristic (ROC) curve was obtained to clarify the diagnostic potency of studied miRNAs. The differentially expressed miRNA profiles and corresponding biological activities were predicted in accordance with bioinformatics data. Targeted miRNAs' expression profiles displayed a significant difference between COVID-19 subjects with normal and abnormal coagulation indices. Moreover, the average miR-223-3p level expressed in COVID-19 cases with normal coagulation indices was significantly lower than that in healthy controls. Based on data from ROC analysis, miR-223-3p and miR-494-3p are promising biomarkers to distinguish the COVID-19 cases with normal or abnormal coagulation indices. Bioinformatics data highlighted the prominent role of selected miRNAs in the inflammation and TGF-beta signaling pathway. The differences existed in the expression profiles of selected miRNAs between the groups introduced miR-494-3p and miR-223-3p as potent biomarkers to prognosis the incidence of COVID-19.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

qRT-PCR:

Quantitative real-time polymerase chain reactions

COVID-19:

Coronavirus disease of 2019

ROC:

Receiver operating characteristic

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

ssRNA:

Single-strand RNA viruses

ARDS:

Acute respiratory distress syndrome

ACE2:

Angiotensin-converting enzyme 2

TNF-α:

Tumor necrosis factor alpha

DIC:

Disseminated intravascular coagulation

TF:

Tissue factor

NF-κB:

Nuclear factor kappa-light-chain-enhancer of activated B cells

IL-2:

Interleukin-2

RdRp:

RNA-dependent RNA polymerase

STRING:

Search tool for the retrieval of interacting genes/proteins

IFITM1:

IFN-induced transmembrane protein 1

STAT:

Signal transducer and activator of transcription

RIG-I:

Retinoic acid-inducible gene I

ZMAT3:

Zinc finger matrin-type 3

MXD1:

MAX dimerization protein 1

ESR1:

Estrogen receptor 1

RRAGD:

Ras related GTP binding D

NFIA:

Nuclear factor I A

References

  1. Rasizadeh R, Baghi HB (2023) Increase in rabies cases during COVID-19 pandemic: Is there a connection? J Infect Dev Count 17:335–336

    Google Scholar 

  2. Eslami N, Aghbash PS, Shamekh A, Entezari-Maleki T, Nahand JS, Sales AJ, Baghi HB (2022) SARS-CoV-2: receptor and co-receptor tropism probability. Curr Microbiol 79:1–13

    Google Scholar 

  3. Hamidi Z, Jabraeili-Siahroud S, Taati-Alamdari Y, Aghbash PS, Shamekh A, Baghi HB (2023) A comprehensive review of COVID-19 symptoms and treatments in the setting of autoimmune diseases. Virology Journal 20:1–11

    PubMed  PubMed Central  Google Scholar 

  4. Hong L-Z, Shou Z-X, Zheng D-M, ** X (2021) The most important biomarker associated with coagulation and inflammation among COVID-19 patients. Mol Cell Biochem 476:2877–2885

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Farzi R, Aghbash PS, Eslami N, Azadi A, Shamekh A, Hemmat N, Entezari-Maleki T, Baghi HB (2022) The role of antigen-presenting cells in the pathogenesis of COVID-19. Pathol Res Pract 233:153848

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Biswas S, Thakur V, Kaur P, Khan A, Kulshrestha S, Kumar P (2021) Blood clots in COVID-19 patients: simplifying the curious mystery. Med Hypotheses 146:110371

    CAS  PubMed  Google Scholar 

  7. Connors JM, Levy JH (2020) COVID-19 and its implications for thrombosis and anticoagulation. Blood 135:2033–2040

    CAS  PubMed  Google Scholar 

  8. Atallah B, Mallah SI, AlMahmeed W (2020) Anticoagulation in COVID-19. Eur Heart J Cardiovasc Pharmacotherapy 6:260–261

    Google Scholar 

  9. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395:497–506

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Boroumand H, Badie F, Mazaheri S, Seyedi ZS, Nahand JS, Nejati M, Baghi HB, Abbasi-Kolli M, Badehnoosh B, Ghandali M (2021) Chitosan-based nanoparticles against viral infections. Front Cell Infect Microbiol 11:643953

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Hum C, Loiselle J, Ahmed N, Shaw TA, Toudic C, Pezacki JP (2021) MicroRNA mimics or inhibitors as antiviral therapeutic approaches against COVID-19. Drugs 81:517–531

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Momekov G, Momekova D (2020) Ivermectin as a potential COVID-19 treatment from the pharmacokinetic point of view: antiviral levels are not likely attainable with known dosing regimens. Biotechnol Biotechnol Equip 34:469–474

    CAS  Google Scholar 

  13. Hemmat N, Mokhtarzadeh A, Aghazadeh M, Jadidi-Niaragh F, Baradaran B, Bannazadeh Baghi H (2020) Role of microRNAs in epidermal growth factor receptor signaling pathway in cervical cancer. Mol Biol Rep 47:4553–4568

    CAS  PubMed  Google Scholar 

  14. Donyavi T, Bokharaei-Salim F, Baghi HB, Khanaliha K, Janat-Makan MA, Karimi B, Nahand JS, Mirzaei H, Khatami A, Garshasbi S (2021) Acute and post-acute phase of COVID-19: analyzing expression patterns of miRNA-29a-3p, 146a-3p, 155-5p, and let-7b-3p in PBMC. Int Immunopharmacol 97:107641

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Jankowska KI, Sauna ZE, Atreya CD (2020) Role of microRNAs in hemophilia and thrombosis in humans. Int J Mol Sci 21:3598

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Vossen CY, van Hylckama VA, Teruel-Montoya R, Salloum-Asfar S, de Haan H, Corral J, Reitsma P, Koeleman BP, Martínez C (2017) Identification of coagulation gene 3′ UTR variants that are potentially regulated by microRNAs. Br J Haematol 177:782–790

    CAS  PubMed  Google Scholar 

  17. Ali HO, Arroyo AB, González-Conejero R, Stavik B, Iversen N, Sandset PM, Martínez C, Skretting G (2016) The role of microRNA-27a/b and microRNA-494 in estrogen-mediated downregulation of tissue factor pathway inhibitor α. J Thromb Haemost 14:1226–1237

    CAS  PubMed  Google Scholar 

  18. Yu X (2021) Another new application of heparin in COVID-19: more than anticoagulation and antiviral. J Invest Med 69:1258

    Google Scholar 

  19. Zhang X, Yu H, Lou JR, Zheng J, Zhu H, Popescu N-I, Lupu F, Lind SE, Ding W-Q (2011) MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem 286:1429–1435

    CAS  PubMed  Google Scholar 

  20. Li S, Chen H, Ren J, Geng Q, Song J, Lee C, Cao C, Zhang J, Xu NJA (2014) MicroRNA-223 inhibits tissue factor expression in vascular endothelial cells. Atherosclerosis 237:514–520

    CAS  PubMed  Google Scholar 

  21. Eisenreich A, Rauch U (2013) Regulation of the tissue factor isoform expression and thrombogenicity of HMEC-1 by miR-126 and miR-19a. Cell Biol: Res Ther 2(1):2

    Google Scholar 

  22. Zhang R, Lu S, Yang X, Li M, Jia H, Liao J, **g Q, Wu Y, Wang H, **ao F (2021) miR-19a-3p downregulates tissue factor and functions as a potential therapeutic target for sepsis-induced disseminated intravascular coagulation. Biochem Pharmacol 192:114671

    CAS  PubMed  Google Scholar 

  23. Haneklaus M, Gerlic M, O’Neill LA, Masters S (2013) miR-223: infection, inflammation and cancer. J Intern Med 274:215–226

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Edén D (2020) Tissue factor regulation, signaling and functions beyond coagulation with a focus on diabetes. Dissertation, Acta Universitatis Upsaliensis

  25. Patel N, Tahara SM, Malik P, Kalra VK (2011) Involvement of miR-30c and miR-301a in immediate induction of plasminogen activator inhibitor-1 by placental growth factor in human pulmonary endothelial cells. Biochem J 434:473–482

    CAS  PubMed  Google Scholar 

  26. Hirahata M, Osaki M, Kanda Y, Sugimoto Y, Yoshioka Y, Kosaka N, Takeshita F, Fujiwara T, Kawai A, Ito H (2016) PAI-1, a target gene of miR-143, regulates invasion and metastasis by upregulating MMP-13 expression of human osteosarcoma. Cancer Med 5:892–902

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Lui W (2016) Characterisation of miR-494 in coagulation. Dissertation, Murdoch University

  28. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    CAS  PubMed  Google Scholar 

  29. Ramakers C, Ruijter JM, Deprez RHL, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    CAS  PubMed  Google Scholar 

  30. Zeng C, Waheed AA, Li T, Yu J, Zheng Y-M, Yount JS, Wen H, Freed EO, Liu S-L (2021) SERINC proteins potentiate antiviral type I IFN production and proinflammatory signaling pathways. Sci Signal 14:eabc7611

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Rosa A, Ballarino M, Sorrentino A, Sthandier O, De Angelis F, Marchioni M, Masella B, Guarini A, Fatica A, Peschle C (2007) The interplay between the master transcription factor PU. 1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci 104:19849–19854

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Wu YZ, Chan KYY, Leung KT, Lam HS, Tam YH, Lee KH, Li K, Ng PC (2021) The miR-223/nuclear factor I-A axis regulates inflammation and cellular functions in intestinal tissues with necrotizing enterocolitis. FEBS Open Bio 11:1907–1920

    PubMed  PubMed Central  Google Scholar 

  33. Hu Y-W, Zhao J-Y, Li S-F, Huang J-L, Qiu Y-R, Ma X, Wu S-G, Chen Z-P, Hu Y-R, Yang J-Y (2015) RP5-833A20. 1/miR-382-5p/NFIA-dependent signal transduction pathway contributes to the regulation of cholesterol homeostasis and inflammatory reaction. Arterioscl Thrombosis Vasc Biol 35:87–101

    CAS  Google Scholar 

  34. Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, Nojima A, Nabetani A, Oike Y, Matsubara H (2009) A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat Med 15:1082–1087

    CAS  PubMed  Google Scholar 

  35. Vilborg A, Glahder JA, Wilhelm MT, Bersani C, Corcoran M, Mahmoudi S, Rosenstierne M, Grandér D, Farnebo M, Norrild B (2009) The p53 target Wig-1 regulates p53 mRNA stability through an AU-rich element. Proc Natl Acad Sci 106:15756–15761

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Spinelli R, Florese P, Parrillo L, Zatterale F, Longo M, D’Esposito V, Desiderio A, Nerstedt A, Gustafson B, Formisano P (2022) ZMAT3 hypomethylation contributes to early senescence of preadipocytes from healthy first-degree relatives of type 2 diabetics. Aging Cell 21:e13557

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Camaioni C, Gustapane M, Cialdella P, Della Bona R, Biasucci LMJI, Medicine E (2013) Microparticles and microRNAs: new players in the complex field of coagulation. Intern Emergency Med 8:291–296

    Google Scholar 

  38. Salloum-Asfar S, Teruel-Montoya R, Arroyo AB, García-Barberá N, Chaudhry A, Schuetz E, Luengo-Gil G, Vicente V, González-Conejero R, Martínez CJPO (2014) Regulation of coagulation factor XI expression by microRNAs in the human liver. PLoS ONE 9:e111713

    PubMed  PubMed Central  Google Scholar 

  39. Jose RJ, Manuel A (2020) COVID-19 cytokine storm: the interplay between inflammation and coagulation. Lancet Respir Med 8:e46–e47

    CAS  PubMed  Google Scholar 

  40. Milenkovic M, Hadzibegovic A, Kovac M, Jovanovic B, Stanisavljevic J, Djikic M, Sijan D, Ladjevic N, Palibrk I, Djukanovic M (2022) D-dimer, CRP, PCT, and IL-6 levels at admission to ICU can predict in-hospital mortality in patients with COVID-19 pneumonia. Oxidat Med Cell Long 2022:1

    Google Scholar 

  41. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, **ang J, Wang Y, Song B, XJTI Gu (2020) Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 395:1054–1062

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Tang N, Li D, Wang X, Sun Z (2020) Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost 18:844–847

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Fayyad-Kazan M, Makki R, Skafi N, El Homsi M, Hamade A, El Majzoub R, Hamade E, Fayyad-Kazan H, Badran B (2021) Circulating miRNAs: potential diagnostic role for coronavirus disease 2019 (COVID-19). Infect Genet Evol 94:105020

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Oto J, Navarro S, Larsen AC, Solmoirago MJ, Plana E, Hervás D, Fernández-Pardo Á, España F, Kristensen SR, Thorlacius-Ussing O (2020) MicroRNAs and neutrophil activation markers predict venous thrombosis in pancreatic ductal adenocarcinoma and distal extrahepatic cholangiocarcinoma. Int J Mol Sci 21:840

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Chen H, Li X, Liu S, Gu L, Zhou X (2017) MircroRNA-19a promotes vascular inflammation and foam cell formation by targeting HBP-1 in atherogenesis. Sci Rep 7:12089

    PubMed  PubMed Central  Google Scholar 

  46. Chow JT, Salmena L (2020) Prediction and analysis of SARS-CoV-2-Targeting MicroRNA in human lung epithelium. Genes (Basel) 2020:11

    Google Scholar 

  47. Arghiani N, Nissan T, Matin MMJB, Pharmacotherapy (2021) Role of microRNAs in COVID-19 with implications for therapeutics. Biomed Pharmacother 144:112247

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Villadsen S, Bramsen J, Ostenfeld M, Wiklund E, Fristrup N, Gao S, Hansen T, Jensen T, Borre M, Ørntoft TJBjoc (2012) The miR-143/-145 cluster regulates plasminogen activator inhibitor-1 in bladder cancer. Br J Cancer 106:366–374

    CAS  PubMed  Google Scholar 

  49. Tiedt S, Prestel M, Malik R, Schieferdecker N, Duering M, Kautzky V, Stoycheva I, Böck J, Northoff BH, Klein MJCR (2017) RNA-Seq identifies circulating miR-125a-5p, miR-125b-5p, and miR-143-3p as potential biomarkers for acute ischemic stroke. Circ Res 121:970–980

    CAS  PubMed  Google Scholar 

  50. Zeng Z, **a L, Fan X, Ostriker AC, Yarovinsky T, Su M, Zhang Y, Peng X, **e Y, Pi LJTJ (2019) Platelet-derived miR-223 promotes a phenotypic switch in arterial injury repair. J Clin Invest 129:1372–1386

    PubMed  PubMed Central  Google Scholar 

  51. Alexandru N, Constantin A, Nemecz M, Comariţa IK, Vîlcu A, Procopciuc A, Tanko G, Georgescu AJFIM (2019) Hypertension associated with hyperlipidemia induced different microRNA expression profiles in plasma, platelets, and platelet-derived microvesicles; effects of endothelial progenitor cell therapy. Front Med 280:1

    Google Scholar 

  52. Morales L, Oliveros JC, Enjuanes L, Sola IJM (2022) Contribution of host miRNA-223-3p to SARS-CoV-induced lung inflammatory pathology. MBio 13:e03135-e3221

    PubMed  PubMed Central  Google Scholar 

  53. Rezk N, Elsayed Sileem A, Gad D, Khalil AOJZUMJ (2022) miRNA-223-3p, miRNA-2909 and cytokines expression in COVID-19 patients treated with ivermectin. Zagazig Univ Med J 28:573–582

    CAS  Google Scholar 

  54. Leierseder S, Petzold T, Zhang L, Loyer X, Massberg S, Engelhardt S (2013) MiR-223 is dispensable for platelet production and function in mice. Thromb Haemost 110:1207–1214

    CAS  PubMed  Google Scholar 

  55. Nahand JS, Karimzadeh MR, Nezamnia M, Fatemipour M, Khatami A, Jamshidi S, Moghoofei M, Taghizadieh M, Hajighadimi S, Shafiee AJIL (2020) The role of miR-146a in viral infection. IUBMB Life 72:343–360

    CAS  PubMed  Google Scholar 

  56. Letafati A, Najafi S, Mottahedi M, Karimzadeh M, Shahini A, Garousi S, Abbasi-Kolli M, Sadri Nahand J, Tamehri Zadeh SS, Hamblin MRJC, Letters MB (2022) MicroRNA let-7 and viral infections: focus on mechanisms of action. Cell Mol Biol Lett 27:1–47

    Google Scholar 

  57. Jafarzadeh A, Naseri A, Shojaie L, Nemati M, Jafarzadeh S, Baghi HB, Hamblin MR, Akhlagh SA, Mirzaei HJII (2021) MicroRNA-155 and antiviral immune responses. Int Immunopharmacol 101:108188

    CAS  PubMed  Google Scholar 

  58. Nahand JS, Shojaie L, Akhlagh SA, Ebrahimi MS, Mirzaei HR, Baghi HB, Mahjoubin-Tehran M, Rezaei N, Hamblin MR, Tajiknia VJMT-NA (2021) Cell death pathways and viruses: role of microRNAs. Mol Therapy Nucl Acids 24:487–511

    Google Scholar 

  59. Hazra B, Kumawat KL, Basu A (2017) The host microRNA miR-301a blocks the IRF1-mediated neuronal innate immune response to Japanese encephalitis virus infection. Sci Signal 10:eaaf5185

    PubMed  Google Scholar 

  60. Hazra B, Chakraborty S, Bhaskar M, Mukherjee S, Mahadevan A, Basu A (2019) miR-301a regulates inflammatory response to japanese encephalitis virus infection via suppression of NKRF activity. J Immunol (Baltimore, Md: 1950) 203:2222–2238

    CAS  Google Scholar 

  61. Jankowska KI, Sauna ZE, Atreya CD (2020) Role of microRNAs in hemophilia and thrombosis in humans. Int J Mol Sci 21:1

    Google Scholar 

  62. He C, Shi Y, Wu R, Sun M, Fang L, Wu W, Liu C, Tang M, Li Z, Wang PJG (2016) miR-301a promotes intestinal mucosal inflammation through induction of IL-17A and TNF-α in IBD. Gut 65:1938–1950

    CAS  PubMed  Google Scholar 

  63. Parray A, Mir F, Doudin A, Iskandarani A, Danjuma IM, Kuni R, Abdelmajid A, Abdelhafez I, Arif R, Mulhim M (2021) Blood snoRNAs and miRNAs as predictors of COVID-19 Severity. Res Square 2021:1

    Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This project was supported by the Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran (IR.TBZMED.REC.1401.276), and Iraqi Ministry of Higher Education and Scientific Research, Iraq.

Author information

Authors and Affiliations

  1. Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, 5166/15731, Iran

    Ammar Khalo Abass Kasho, Javid Sadri Nahand, Ahad Bazmani & Hossein Bannazadeh Baghi

  2. Iraqi Ministry of Higher Education and Scientific Research, Tal Afar University, Tal Afar, Iraq

    Ammar Khalo Abass Kasho

  3. Department of Plant Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran

    Ammar Khalo Abass Kasho & Nader Farsad-Akhtar

  4. Regenerative Medicine, Organ Procurement and Transplantation Multi-Disciplinary Center, Razi Hospital, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Arash Salmaninejad

  5. Department of Medical Genetics, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Arash Salmaninejad

  6. Research Center for Biochemistry and Nutrition in Metabolic Diseases, Institute for Basic Sciences, Kashan University of Medical Sciences, Kashan, Iran

    Hamed Mirzaei

  7. Infectious Diseases Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Mohsen Moghoofei

  8. Department of Microbiology, Faculty of Medicine, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Mohsen Moghoofei

  9. Immunology Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Parisa Shiri Aghbash, Reyhaneh Rasizadeh & Hossein Bannazadeh Baghi

  10. Department of Virology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Parisa Shiri Aghbash, Reyhaneh Rasizadeh & Hossein Bannazadeh Baghi

Authors
  1. Ammar Khalo Abass Kasho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javid Sadri Nahand
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arash Salmaninejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hamed Mirzaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohsen Moghoofei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ahad Bazmani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Parisa Shiri Aghbash
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Reyhaneh Rasizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nader Farsad-Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hossein Bannazadeh Baghi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NF and HBB design the experiments and supervised the research. AKHAK, JSN, AS, HM, MM, carried out the experiment, analyzed data, wrote and revised the manuscript. AB, PSH and RR contributed to the data collection and drafting of the manuscript. Each scholar verified the resulting version to submit the paper.

Corresponding authors

Correspondence to Nader Farsad-Akhtar or Hossein Bannazadeh Baghi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest to report.

Consent for Publication

Not applicable.

Ethics Approval and Consent to Participate

The research protocol was approved by the Medical Ethics Committee of Tabriz University of Medical Sciences, Iran (IR.TBZMED.REC.1401.276). All research units signed an informed written consent according to the declaration of Helsinki.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kasho, A.K.A., Nahand, J.S., Salmaninejad, A. et al. PBMC MicroRNAs: Promising Biomarkers for the Differential Diagnosis of COVID-19 Patients with Abnormal Coagulation Indices. Curr Microbiol 80, 248 (2023). https://doi.org/10.1007/s00284-023-03365-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03365-2

Search

Navigation