2,589
Views
9
CrossRef citations to date
0
Altmetric
Research Article

Zika virus promotes CCN1 expression via the CaMKIIα-CREB pathway in astrocytes

, , , , , , , , , ORCID Icon, , & ORCID Icon show all
Pages 113-131 | Received 27 Apr 2019, Accepted 22 Nov 2019, Published online: 20 Jan 2020

References

  • Pierson TC, Graham BS. Zika virus: immunity and vaccine development. Cell. 2016;167(3):625–631.
  • Retallack H, Di Lullo E, Arias C, et al. Zika virus in the human placenta and developing brain: cell tropism and drug inhibition. bioRxiv. 2016; p. 058883.
  • Detje CN, Lienenklaus S, Chhatbar C, et al. Upon intranasal vesicular stomatitis virus infection, astrocytes in the olfactory bulb are important interferon Beta producers that protect from lethal encephalitis. J Virol. 2015;89(5):2731–2738.
  • Reinert LS, Harder L, Holm CK, et al. TLR3 deficiency renders astrocytes permissive to herpes simplex virus infection and facilitates establishment of CNS infection in mice. J Clin Investig. 2012;122(4):1368–1376.
  • Carsten K, Ackerman A, Lienenklaus S, et al. Visualizing production of beta interferon by astrocytes and microglia in brain of La Crosse virus-infected mice. J Virol. 2012;86(20):11223–11230.
  • Lindqvist R, Mundt F, Gilthorpe JD, et al. Fast type I interferon response protects astrocytes from flavivirus infection and virus-induced cytopathic effects. J Neuroinflammation. 2016;13(1):277.
  • Norenberg MD. Astrocyte responses to CNS injury. J Neuropathol Exp Neurol. 1994;53(3):213–220.
  • Bush TG, Puvanachandra N, Horner CH, et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron. 1999;23(2):297–308.
  • Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7(1):41–53.
  • Almad A, Maragakis NJ. A stocked toolbox for understanding the role of astrocytes in disease. Nat Rev Neurol. 2018;14:351–362.
  • Potokar M, Jorgacevski J, Zorec R. Astrocytes in Flavivirus Infections. Int J Mol Sci. 2019;20(3):691.
  • Lossia OV, Conway MJ, Tree MO, et al. Zika virus induces astrocyte differentiation in neural stem cells. J Neurovirol. 2018;24(1):52–61.
  • Chen J, Yang Y-F, Yang Y, et al. AXL promotes Zika virus infection in astrocytes by antagonizing type I interferon signalling. Nat Microbiol. 2018;3(3):302.
  • Cheng F, Ramos da Silva S, Huang I-C, et al. Suppression of Zika virus infection and replication in endothelial cells and astrocytes by PKA inhibitor PKI 14-22. J Virol. 2018;92(4):e02019–17.
  • Kozak R, Majer A, Biondi M, et al. MicroRNA and mRNA dysregulation in astrocytes infected with Zika virus. Viruses. 2017;9(10):297.
  • Limonta D, Jovel J, Kumar A, et al. Human fetal astrocytes infected with Zika Virus exhibit delayed apoptosis and resistance to interferon: implications for persistence. Viruses. 2018;10(11):646.
  • Lulu Y, Brahim C. Cysteine-rich protein 61 (CCN1) and connective tissue growth factor (CCN2) at the crosshairs of ocular neovascular and fibrovascular disease therapy. J Cell Commun Signal. 2013;7(4):253–263.
  • Yang R, Chen Y, Chen D. Biological functions and role of CCN1/Cyr61 in embryogenesis and tumorigenesis in the female reproductive system (Review). Mol Med Rep. 2018;17(1):3–10.
  • Perbal B. The concept of the CCN protein family revisited: a centralized coordination network. J Cell Commun Signal. 2018;12(1):3–12.
  • Borkham-Kamphorst E, Steffen BT, Van de Leur E, et al. CCN1/CYR61 overexpression in hepatic stellate cells induces ER stress-related apoptosis. Cell Signal. 2015;28(1):34–42.
  • Joon-Il J, Lau LF. Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov. 2011;10(12):945.
  • Wu P, Ma G, Zhu X, et al. Cyr61/CCN1 is involved in the pathogenesis of psoriasis vulgaris via promoting IL-8 production by keratinocytes in a JNK/NF-κB pathway. Clin Immunol. 2017;174:53–62.
  • Shi L, Dong N, Ji D, et al. Lipopolysaccharide-induced CCN1 production enhances interleukin-6 secretion in bronchial epithelial cells. Cell Biol Toxicol. 2018;34(1):39–49.
  • Johannes G, Carter MS, Eisen MB, et al. Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc Natl Acad Sci U S A. 1999;96(23):13118–13123.
  • Kim S-M, Park J-H, Chung S-K, et al. Coxsackievirus B3 infection induces cyr61 activation via JNK to mediate cell death. J Virol. 2004;78(24):13479–13488.
  • Kurozumi K, Hardcastle J, Thakur R, et al. Oncolytic HSV-1 Infection of Tumors Induces Angiogenesis and Upregulates CYR61. Mol Ther. 2008;16(8):1382–1391.
  • Moon H-G, Qin Z, Quan T, et al. Matrix protein CCN1 induced by bacterial DNA and CpG ODN limits lung inflammation and contributes to innate immune homeostasis. Mucosal Immunol. 2015;8(2):243–253.
  • Kok S-H, Hou K-L, Hong C-Y, et al. Simvastatin inhibits cytokine‐stimulated Cyr61 expression in osteoblastic cells: A therapeutic benefit for arthritis. Arthritis Rheum. 2011;63(4):1010–1020.
  • Baek A, Park EJ, Kim SY, et al. High-frequency repetitive magnetic stimulation enhances the expression of brain-derived neurotrophic factor through activation of Ca 2+ -calmodulin-dependent protein kinase II-cAMP-response element-binding protein pathway. Front Neurol. 2018;9:285.
  • Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 2002;3(3):175–190.
  • Gaertner‡ TR, Kolodziej SJ, Wang D, et al. Comparative analyses of the 3-Dimensional structures and enzymatic properties of α, β, γ and δ Isoforms of Ca2+-calmodulin dependent protein kinase II. J Biol Chem. 2004;279:12484–12494.
  • Liu X, Zhang L, Jin L, et al. HCN2 contributes to oxaliplatin-induced neuropathic pain through activation of the CaMKII/CREB cascade in spinal neurons. Mol Pain. 2018;14:174480691877849.
  • Zhao J, Wang B, Wang X, et al. Up-regulation of Ca2+/CaMKII/CREB signaling in salicylate-induced tinnitus in rats. Mol Cell Biochem. 2018;448(1–2):1–6.
  • Deng C, Liu S, Zhang Q, et al. Isolation and characterization of Zika virus imported to China using C6/36 mosquito cells. Virol Sin. 2016;31(2):176–179.
  • Lindenbach BD. Measuring HCV infectivity produced in cell culture and in vivo. Methods Mol Biol. 2009;510(510):329.
  • Zhang X, Zheng Z, Liu X, et al. Tick-borne encephalitis virus induces chemokine RANTES expression via activation of IRF-3 pathway. J Neuroinflammation. 2016;13(1):209.
  • Li F, Nellaker C, Sabunciyan S, et al. Transcriptional derepression of the ERVWE1 locus following influenza A virus infection. J Virol. 2014;88(8):4328.
  • Retallack H, Di Lullo E, Arias C, et al. Zika virus cell tropism in the developing human brain and inhibition by azithromycin. Proc Natl Acad Sci U S A. 2016;113(50):201618029.
  • Tan ZY, Zhang WP, Sun JH, et al. ZIKV infection activates the IRE1-XBP1 and ATF6 pathways of unfolded protein response in neural cells. J Neuroinflammation. 2018;15(1):275.
  • Tsai MS, Hornby AE, Lakins J, et al. Expression and function of CYR61, an angiogenic factor, in breast cancer cell lines and tumor biopsies. Cancer Res. 2000;60(20):5603–5607.
  • Shr-Jeng JL, Sung J-S, Huang M-L, et al. A novel anti-CCN1 monoclonal antibody suppresses Rac-dependent cytoskeletal reorganization and migratory activities in breast cancer cells. Biochem Biophys Res Commun. 2013;434(4):885–891.
  • Lothrop D, Nicholson BL. Inhibition of cellular DNA synthesis in cells infected with infectious pancreatic necrosis virus. J Virol. 1974;14(3):485.
  • Johnsen IB, Bergstroem B, Stiberg KA, et al. Inducible cAMP early repressor (ICER) is a novel regulator of RIG-I mediated IFN-β production. Cell Signal. 2013;25(9):1804–1812.
  • Du F, Saitoh F, Tian Q-B, et al. Mechanisms for association of Ca2+/calmodulin-dependent protein kinase II with lipid rafts. Biochem Biophys Res Commun. 2006;347(3):814–820.
  • Wei G, Chen Y-B, Chen D-F, et al. β-Asarone inhibits neuronal apoptosis via the CaMKII/CREB/Bcl-2 signaling pathway in an in vitro model and AβPP/PS1 Mice. J Alzheimers Dis. 2013;33(3):863–880.
  • Li J, Zhao S-Z, Wang -P-P, et al. Calcium mediates high glucose-induced HIF-1α and VEGF expression in cultured rat retinal Müller cells through CaMKII-CREB pathway. Acta Pharmacol Sin. 2012;33(8):1030.
  • Gueugnon F, Thibault VC, Kearley J, et al. Altered expression of the CCN genes in the lungs of mice in response to cigarette smoke exposure and viral and bacterial infections. Gene. 2016;586(1):176–183.
  • Rossi SL, Tesh RB, Azar SR, et al. Characterization of a novel murine model to study Zika Virus. Am J Trop Med Hyg. 2016;94(6):1362–1369.
  • Zhang Y, Sloan S, Clarke L, et al. Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron. 2016;89(1):37–53.
  • Bleau AM, Planque N, Perbal B. CCN proteins and cancer: two to tango. Front Biosci. 2005;10(1–3):998.
  • Sun Y, Zhang J, Zhou Z, et al. CCN1, a pro-inflammatory factor, aggravates psoriasis skin lesions by promoting keratinocyte activation. J Invest Dermatol. 2015;135(11):2666–2675.
  • Su J, Chiou J, Tang C-H, et al. CYR61 Regulates BMP-2-dependent osteoblast differentiation through the αvβ3 Integrin/Integrin-linked Kinase/ERK Pathway. J Biol Chem. 2010;285(41):31325.
  • Xie D, Yin D, Tong X, et al. Cyr61 is overexpressed in gliomas and involved in integrin-linked kinase-mediated Akt and beta-catenin-TCF/Lef signaling pathways. Cancer Res. 2004;64(6):1987–1996.
  • Tan TW, Yang WH, Lin YT, et al. Cyr61 increases migration and MMP-13 expression via alphavbeta3 integrin, FAK, ERK and AP-1-dependent pathway in human chondrosarcoma cells. Carcinogenesis. 2009;30(2):258–268.
  • Emre Y, Imhof BA. Matricellular protein CCN1/CYR61: a new player in inflammation and leukocyte trafficking. Semin Immunopathol. 2014;36(2):253–259.
  • Tangsongcharoen C, Roytrakul S, Smith DR. Analysis of cellular proteome changes in response to ZIKV NS2B-NS3 protease expression. Biochim Biophys Acta Proteins Proteom. 2019;1867(2):89–97.
  • Luo D, Vasudevan S, Lescar J. The flavivirus NS2B-NS3 protease-helicase as a target for antiviral drug development. Antiviral Res. 2015;118:148–158.
  • Latinkic BV, O’Brien TP, Lau LF. Promoter function and structure of the growth factor-inducible immediate early gene cyr61. Nucleic Acids Res. 1991;19(12):3261–3267.
  • Ji-Soo H, Edward M, Joel R, et al. Regulation of Cyr61/CCN1 gene expression through RhoA GTPase and p38MAPK signaling pathways. Eur J Biochem. 2003;270:3408–3421.
  • Cesare DD, Fimia GM, Sassone-Corsi P. Signaling routes to CREM and CREB: plasticity in transcriptional activation. Trends Biochem Sci. 1999;24(7):281–285.
  • Andy H, Howard S. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J. 2002;364(3):593–611.
  • Giese KP, Fedorov NB, Filipkowski RK, et al. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science. 1998;279(5352):870–873.
  • Kawasaki Y, Kohno T, Zhuang ZY, et al. Ionotropic and metabotropic receptors, Protein Kinase A, Protein Kinase C, and Src Contribute to C-Fiber-Induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci Off J Soc Neurosci. 2004;24(38):8310.
  • Gordana M, Pankratz MT, Vjekoslav M. Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats. Pain. 2002;99(3):493–500.
  • Katano T, Nakazawa T, Nakatsuka T, et al. Involvement of spinal phosphorylation cascade of Tyr1472-NR2B, Thr286-CaMKII, and Ser831-GluR1 in neuropathic pain. Neuropharmacology. 2011;60(4):609–616.
  • Singh MV, Anderson ME. Is CaMKII a link between inflammation and hypertrophy in heart? J Mol Med. 2011;89(6):537–543.