HCV-Associated Exosomes Upregulate RUNXOR and RUNX1 Expressions to Promote MDSC Expansion and Suppressive Functions through STAT3-miR124 Axis
RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related transcription factor 1 (RUNX1). We and others have previously reported that myeloid-derived suppressor cells (MDSCs) expand and inhibit host immune resp...
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| Published in | Cells (Basel, Switzerland) Vol. 9; no. 12; p. 2715 |
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| Main Authors | , , , , , , , , , , , , , , , , |
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| Abstract | RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related transcription factor 1 (RUNX1). We and others have previously reported that myeloid-derived suppressor cells (MDSCs) expand and inhibit host immune responses during chronic viral infections; however, the mechanisms responsible for MDSC differentiation and suppressive functions, in particular the role of RUNXOR-RUNX1, remain unclear. Here, we demonstrated that RUNXOR and RUNX1 expressions are significantly upregulated and associated with elevated levels of immunosuppressive molecules, such as arginase 1 (Arg1), inducible nitric oxide synthase (iNOS), signal transducer and activator of transcription 3 (STAT3), and reactive oxygen species (ROS) in MDSCs during chronic hepatitis C virus (HCV) infection. Mechanistically, we discovered that HCV-associated exosomes (HCV-Exo) can induce the expressions of RUNXOR and RUNX1, which in turn regulates miR-124 expression via STAT3 signaling, thereby promoting MDSC differentiation and suppressive functions. Importantly, overexpression of RUNXOR in healthy CD33
myeloid cells promoted differentiation and suppressive functions of MDSCs. Conversely, silencing RUNXOR or RUNX1 expression in HCV-derived CD33
myeloid cells significantly inhibited their differentiation and expressions of suppressive molecules and improved the function of co-cultured autologous CD4 T cells. Taken together, these results indicate that the RUNXOR-RUNX1-STAT3-miR124 axis enhances the differentiation and suppressive functions of MDSCs and could be a potential target for immunomodulation in conjunction with antiviral therapy during chronic HCV infection. |
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| AbstractList | RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related transcription factor 1 (RUNX1). We and others have previously reported that myeloid-derived suppressor cells (MDSCs) expand and inhibit host immune responses during chronic viral infections; however, the mechanisms responsible for MDSC differentiation and suppressive functions, in particular the role of RUNXOR–RUNX1, remain unclear. Here, we demonstrated that RUNXOR and RUNX1 expressions are significantly upregulated and associated with elevated levels of immunosuppressive molecules, such as arginase 1 (Arg1), inducible nitric oxide synthase (iNOS), signal transducer and activator of transcription 3 (STAT3), and reactive oxygen species (ROS) in MDSCs during chronic hepatitis C virus (HCV) infection. Mechanistically, we discovered that HCV-associated exosomes (HCV-Exo) can induce the expressions of RUNXOR and RUNX1, which in turn regulates miR-124 expression via STAT3 signaling, thereby promoting MDSC differentiation and suppressive functions. Importantly, overexpression of RUNXOR in healthy CD33+ myeloid cells promoted differentiation and suppressive functions of MDSCs. Conversely, silencing RUNXOR or RUNX1 expression in HCV-derived CD33+ myeloid cells significantly inhibited their differentiation and expressions of suppressive molecules and improved the function of co-cultured autologous CD4 T cells. Taken together, these results indicate that the RUNXOR–RUNX1–STAT3–miR124 axis enhances the differentiation and suppressive functions of MDSCs and could be a potential target for immunomodulation in conjunction with antiviral therapy during chronic HCV infection. RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related transcription factor 1 (RUNX1). We and others have previously reported that myeloid-derived suppressor cells (MDSCs) expand and inhibit host immune responses during chronic viral infections; however, the mechanisms responsible for MDSC differentiation and suppressive functions, in particular the role of RUNXOR-RUNX1, remain unclear. Here, we demonstrated that RUNXOR and RUNX1 expressions are significantly upregulated and associated with elevated levels of immunosuppressive molecules, such as arginase 1 (Arg1), inducible nitric oxide synthase (iNOS), signal transducer and activator of transcription 3 (STAT3), and reactive oxygen species (ROS) in MDSCs during chronic hepatitis C virus (HCV) infection. Mechanistically, we discovered that HCV-associated exosomes (HCV-Exo) can induce the expressions of RUNXOR and RUNX1, which in turn regulates miR-124 expression via STAT3 signaling, thereby promoting MDSC differentiation and suppressive functions. Importantly, overexpression of RUNXOR in healthy CD33 myeloid cells promoted differentiation and suppressive functions of MDSCs. Conversely, silencing RUNXOR or RUNX1 expression in HCV-derived CD33 myeloid cells significantly inhibited their differentiation and expressions of suppressive molecules and improved the function of co-cultured autologous CD4 T cells. Taken together, these results indicate that the RUNXOR-RUNX1-STAT3-miR124 axis enhances the differentiation and suppressive functions of MDSCs and could be a potential target for immunomodulation in conjunction with antiviral therapy during chronic HCV infection. RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related transcription factor 1 (RUNX1). We and others have previously reported that myeloid-derived suppressor cells (MDSCs) expand and inhibit host immune responses during chronic viral infections; however, the mechanisms responsible for MDSC differentiation and suppressive functions, in particular the role of RUNXOR–RUNX1, remain unclear. Here, we demonstrated that RUNXOR and RUNX1 expressions are significantly upregulated and associated with elevated levels of immunosuppressive molecules, such as arginase 1 (Arg1), inducible nitric oxide synthase (iNOS), signal transducer and activator of transcription 3 (STAT3), and reactive oxygen species (ROS) in MDSCs during chronic hepatitis C virus (HCV) infection. Mechanistically, we discovered that HCV-associated exosomes (HCV-Exo) can induce the expressions of RUNXOR and RUNX1, which in turn regulates miR-124 expression via STAT3 signaling, thereby promoting MDSC differentiation and suppressive functions. Importantly, overexpression of RUNXOR in healthy CD33 + myeloid cells promoted differentiation and suppressive functions of MDSCs. Conversely, silencing RUNXOR or RUNX1 expression in HCV-derived CD33 + myeloid cells significantly inhibited their differentiation and expressions of suppressive molecules and improved the function of co-cultured autologous CD4 T cells. Taken together, these results indicate that the RUNXOR–RUNX1–STAT3–miR124 axis enhances the differentiation and suppressive functions of MDSCs and could be a potential target for immunomodulation in conjunction with antiviral therapy during chronic HCV infection. |
| Author | Nguyen, Lam N Cao, Dechao Zhao, Juan Zhang, Jinyu Moorman, Jonathan P Thakuri, Bal Krishna Chand Wang, Ling Nguyen, Lam N T Jiang, Yong Dang, Xindi El Gazzar, Mohamed Schank, Madison Ning, Shunbin Lu, Zeyuan Yao, Zhi Q Khanal, Sushant Wu, Xiao Y |
| AuthorAffiliation | 1 Center of Excellence for Inflammation, Infectious Disease and Immunity, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, TN 37614, USA; thakuri@etsu.edu (B.K.C.T.); zhangj2@etsu.edu (J.Z.); zhaoj2@etsu.edu (J.Z.); nguyenl@etsu.edu (L.N.N.); nguyenln@etsu.edu (L.N.T.N.); niecem@etsu.edu (M.S.); khanals@etsu.edu (S.K.); dangx1@etsu.edu (X.D.); caod01@etsu.edu (D.C.); LUZ001@mail.etsu.edu (Z.L.); WUXY@etsu.edu (X.Y.W.); JIANGY2@mail.etsu.edu (Y.J.); ELGAZZAR@etsu.edu (M.E.G.); nings1@etsu.edu (S.N.); wangl3@etsu.edu (L.W.); moorman@etsu.edu (J.P.M.) 3 Hepatitis (HCV/HBV/HIV) Program, James H. Quillen VA Medical Center, Department of Veterans Affairs, Johnson City, TN 37614, USA 2 Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA |
| AuthorAffiliation_xml | – name: 1 Center of Excellence for Inflammation, Infectious Disease and Immunity, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, TN 37614, USA; thakuri@etsu.edu (B.K.C.T.); zhangj2@etsu.edu (J.Z.); zhaoj2@etsu.edu (J.Z.); nguyenl@etsu.edu (L.N.N.); nguyenln@etsu.edu (L.N.T.N.); niecem@etsu.edu (M.S.); khanals@etsu.edu (S.K.); dangx1@etsu.edu (X.D.); caod01@etsu.edu (D.C.); LUZ001@mail.etsu.edu (Z.L.); WUXY@etsu.edu (X.Y.W.); JIANGY2@mail.etsu.edu (Y.J.); ELGAZZAR@etsu.edu (M.E.G.); nings1@etsu.edu (S.N.); wangl3@etsu.edu (L.W.); moorman@etsu.edu (J.P.M.) – name: 2 Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – name: 3 Hepatitis (HCV/HBV/HIV) Program, James H. Quillen VA Medical Center, Department of Veterans Affairs, Johnson City, TN 37614, USA |
| Author_xml | – sequence: 1 givenname: Bal Krishna Chand surname: Thakuri fullname: Thakuri, Bal Krishna Chand organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 2 givenname: Jinyu surname: Zhang fullname: Zhang, Jinyu organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 3 givenname: Juan surname: Zhao fullname: Zhao, Juan organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 4 givenname: Lam N surname: Nguyen fullname: Nguyen, Lam N organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 5 givenname: Lam N T surname: Nguyen fullname: Nguyen, Lam N T organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 6 givenname: Madison surname: Schank fullname: Schank, Madison organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 7 givenname: Sushant orcidid: 0000-0001-8028-6034 surname: Khanal fullname: Khanal, Sushant organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 8 givenname: Xindi surname: Dang fullname: Dang, Xindi organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 9 givenname: Dechao surname: Cao fullname: Cao, Dechao organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 10 givenname: Zeyuan surname: Lu fullname: Lu, Zeyuan organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 11 givenname: Xiao Y surname: Wu fullname: Wu, Xiao Y organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 12 givenname: Yong surname: Jiang fullname: Jiang, Yong organization: Center of Excellence for Inflammation, Infectious Disease and Immunity, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, TN 37614, USA – sequence: 13 givenname: Mohamed surname: El Gazzar fullname: El Gazzar, Mohamed organization: Center of Excellence for Inflammation, Infectious Disease and Immunity, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, TN 37614, USA – sequence: 14 givenname: Shunbin orcidid: 0000-0001-5484-5779 surname: Ning fullname: Ning, Shunbin organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 15 givenname: Ling surname: Wang fullname: Wang, Ling organization: Division of Infectious, Inflammatory and Immunologic Diseases, Department of Internal Medicine, Quillen College of Medicine, ETSU, Johnson City, TN 37614, USA – sequence: 16 givenname: Jonathan P surname: Moorman fullname: Moorman, Jonathan P organization: Hepatitis (HCV/HBV/HIV) Program, James H. Quillen VA Medical Center, Department of Veterans Affairs, Johnson City, TN 37614, USA – sequence: 17 givenname: Zhi Q surname: Yao fullname: Yao, Zhi Q organization: Hepatitis (HCV/HBV/HIV) Program, James H. Quillen VA Medical Center, Department of Veterans Affairs, Johnson City, TN 37614, USA |
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| Keywords | miR124 MDSCs HCV immune suppression RUNX1 RUNXOR |
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| Snippet | RUNX1 overlapping RNA (RUNXOR) is a long non-coding RNA and plays a pivotal role in the differentiation of myeloid cells via targeting runt-related... |
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| SubjectTerms | Antibodies Antiviral agents Arginase CD4 antigen Cell differentiation Chronic infection Exosomes Flow cytometry HCV Hepatitis C immune suppression Immunomodulation Infections Infectious diseases Lymphocytes Lymphocytes T MDSCs miR124 Myeloid cells Nitric-oxide synthase Non-coding RNA Pathogens Reactive oxygen species RUNX1 Runx1 protein RUNXOR Stat3 protein Suppressor cells Viral infections |
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| Title | HCV-Associated Exosomes Upregulate RUNXOR and RUNX1 Expressions to Promote MDSC Expansion and Suppressive Functions through STAT3-miR124 Axis |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33353065 https://www.proquest.com/docview/2473385722/abstract/ https://search.proquest.com/docview/2473411316 https://pubmed.ncbi.nlm.nih.gov/PMC7766103 https://doaj.org/article/818d5f8ed34e4974a97c10efe95a956c |
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