Glia Maturation Factor Beta: A Novel Neuro-Impairment Prediction Factor in Toxoplasmosis
Abstract
Background: Toxoplasma gondii, a neurotropic protozoan, infects up one to third of the world population. The parasite can invade a wide variety of nucleated cells but preferably glial cells. Glia maturation factor β (GMFβ), a 17KD protein expressed at high levels in the central nervous system is predominantly related to neurodegenerative diseases such as Alzheimer's disease, Parkinson's disease, and Multiple sclerosis. We aimed to determine the expression level of GMFβ and its relation to other pro-inflammatory factors (IL33, SDF1, and CCL2) on T. gondii infected human neuroblastoma cell line.
Methods: The human neuroblastoma (SK_NMC C535) cell line was infected by 5106 (1:1 ratio). The supernatant was collected after cell lysis and centrifugation. Total RNA was extracted using the Yekta Tajhiz RNA extraction kit. cDNA was synthesized based on RevertAid First Strand cDNA Synthesis Kit manufacturer`s protocol (Parstous, cDNA synthesis kit, Iran). The specificity of each primer pair (GMFβ, IL33, SDF1, and CCL2) was provided by NCBI BLAST. Gene expression level was measured using Real-Time PCR. All experiments were conducted at the Hamadan University of Medical Sciences, western Iran in 2022.
Results: The GMFβ increased significantly up to 1.35-fold (P=0.007). The increase in GMFβ expression in neuroblastoma cells was consistent with the increase in pro-inflammatory factors (CCL2 (0.47), IL33 (0.152) and, SDF1 (1.33)).
Conclusion: GMFβ upregulation can be a novel indicator of the destruction of nerve cells.
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19. Berger O, Li G, Han S-M, et al (2007). Expression of SDF-1 and CXCR4 during reorganization of the postnatal dentate gyrus. Dev Neurosci, 29 (1-2):48-58.
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23. Pujol F, Kitabgi P, Boudin H (2005). The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J Cell Sci, 118 (Pt 5):1071-1080.
24. Safronova A, Araujo A, Camanzo ET, et al (2019). Alarmin S100A11 initiates a chemokine response to the human pathogen Toxoplasma gondii. Nat Immunol, 20 (1):64-72.
25. Foroghi parvar F, Keshavarz H, Shojaee S (2007). Detection of Toxoplasma gondii antigens in sera and urine of experimentally infected mice by capture ELISA. Iran J Parasitol, 3 (1):1-5.
26. Jabari S, Keshavarz H, Salimi M, et al (2018). In vitro culture of Toxoplasma gondii in HeLa, Vero, RBK and A549 cell lines. Infez Med, 26 (2):145-147.
27. Karimi Dermani F, Saidijam M, Amini R, et al (2017). Resveratrol inhibits proliferation, invasion, and epithelial–mesenchymal transition by increasing miR‐200c expression in HCT‐116 colorectal cancer cells. J Cell Biochem, 118 (6):1547-1555.
28. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25 (4):402-408.
29. Santana S, Sastre I, Recuero M, et al (2013). Oxidative stress enhances neurodegeneration markers induced by herpes simplex virus type 1 infection in human neuroblastoma cells. PLoS One, 8 (10):e75842.
30. Pontrello CG, McWhirt JM, Glabe CG, et al (2022). Age-Related Oxidative Redox and Metabolic Changes Precede Intraneuronal Amyloid-β Accumulation and Plaque Deposition in a Transgenic Alzheimer’s Disease Mouse Model. J Alzheimers Dis, 90 (4):1501-1521.
31. Mecocci P, Boccardi V, Cecchetti R, et al (2018). A long journey into aging, brain aging, and Alzheimer’s disease following the oxidative stress tracks. J Alzheimers Dis, 62 (3):1319-1335.
32. Clausen A, Xu X, Bi X, Baudry M (2012). Effects of the superoxide dismutase/catalase mimetic EUK-207 in a mouse model of Alzheimer's disease: protection against and interruption of progression of amyloid and tau pathology and cognitive decline. J Alzheimers Dis, 30 (1):183-208.
33. Zheng C, Zhou M, Sun J, et al (2019). The protective effects of liraglutide on AD-like neurodegeneration induced by oxidative stress in human neuroblastoma SH-SY5Y cells. Chem Biol Interact, 310:108688.
34. Najafi M, Amini R, Maghsood AH, et al (2021). Co expression of GMFβ, IL33, CCL2 and SDF1 genes in the acute stage of toxoplasmosis in mice model and relation for neuronal impairment. Iran J Parasitol, 16 (3):426-434.
35. Zaheer A, Zaheer S, Thangavel R, et al (2008). Glia maturation factor modulates β-amyloid-induced glial activation, inflammatory cytokine/chemokine production and neuronal damage. Brain Res, 1208:192-203.
36. Liu C, Sun W, Zhu T, et al (2022). Glia maturation factor-β induces ferroptosis by impairing chaperone-mediated autophagic degradation of ACSL4 in early diabetic retinopathy. Redox Biol, 52:102292.
37. Selvakumar GP, Iyer SS, Kempuraj D, Ahmed ME, et al (2019). Molecular association of glia maturation factor with the autophagic machinery in rat dopaminergic neurons: a role for endoplasmic reticulum stress and MAPK activation. Mol Neurobiol, 56 (6):3865-3881.
38. Dincel GC, Kul O (2019). First description of enhanced expression of transforming growth factor-alpha (TGF-α) and glia maturation factor-beta (GMF-β) correlate with severity of neuropathology in border disease virus-infected small ruminants. Microb Pathog, 128:301-310.
39. Kumar R, Amruthanjali T, Singothu S, et al (2022). Uncoupling proteins as a therapeutic target for the development of new era drugs against neurodegenerative disorder. Biomed Pharmacother, 147:112656.
40. Thangavel R, Van Hoesen GW, Zaheer A (2009). The abnormally phosphorylated tau lesion of early Alzheimer’s disease. Neurochem Res, 34 (1):118-123.
41. Ramaswamy SB, Bhagavan SM, Kaur H, et al (2019). Glia Maturation Factor in the Pathogenesis of Alzheimer’s disease. Open Access J Neurol Neurosurg, 12 (3):79-82.
42. Luan K, Rosales JL, Lee K-Y (2013). Crosstalks between neurofibrillary tangles and amyloid plaque formation. Ageing Res Rev, 12 (1):174-181.
43. Sun W, Hu C, Wang T, et al (2021). Glia maturation factor beta as a novel biomarker and therapeutic target for hepatocellular carcinoma. Front Oncol, 11:744331.
44. Berrett AN, Gale SD, Erickson LD, et al (2017). Toxoplasma gondii moderates the association between multiple folate-cycle factors and cognitive function in US adults. Nutrients, 9 (6):564.
45. Galeh TM, Ghazvini H, Sarvi S, et al (2022). Controversial Effects of Diverse Types of Toxoplasma gondii on the Anxiety-like Behavior and Cognitive Impairments in the Animal Model of Alzheimer's Disease. Iran J Psychiatry Behav Sci, 16 (3) e122961.
46. Castaño Barrios L, Da Silva Pinheiro AP, Gibaldi D, et al (2021). Behavioral alterations in long-term toxoplasma gondii infection of C57BL/6 mice are associated with neuroinflammation and disruption of the blood brain barrier. PLoS One, 16 (10):e0258199.
47. Wen X, Kudo T, Payne L, et al (2010). Predominant interferon-γ-mediated expression of CXCL9, CXCL10, and CCL5 proteins in the brain during chronic infection with Toxoplasma gondii in BALB/c mice resistant to development of toxoplasmic encephalitis. J Interferon Cytokine Res, 30 (9):653-660.
48. Batista SJ, Still KM, Johanson D, et al (2020). Gasdermin-D-dependent IL-1α release from microglia promotes protective immunity during chronic Toxoplasma gondii infection. Nat Commun, 11 (1):3687.
49. Zhang Y, He J, Zheng H, et al (2019). Association of TREM-1, IL-1β, IL-33/ST2, and TLR expressions with the pathogenesis of ocular toxoplasmosis in mouse models on different genetic backgrounds. Front Microbiol, 10:2264.
50. Liew FY, Pitman NI, McInnes IB (2010). Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol, 10 (2):103-110.
51. Cayrol C (2021). IL-33, an alarmin of the IL-1 family involved in allergic and non allergic inflammation: focus on the mechanisms of regulation of its activity. Cells, 11 (1):107.
52. Ryffel B, Huang F, Robinet P, et al (2019). Blockade of IL-33R/ST2 signaling attenuates Toxoplasma gondii Ileitis depending on IL-22 expression. Front Immunol, 10:702.
53. Ryan N, Anderson K, Volpedo G, et al (2020). The IL-33/ST2 axis in immune responses against parasitic disease: potential therapeutic applications. Front Cell Infect Microbiol, 10:153.
54. de Araújo TE, Coelho-dos-Reis JG, Béla SR, et al (2017). Early serum biomarker networks in infants with distinct retinochoroidal lesion status of congenital toxoplasmosis. Cytokine, 95:102-112.
55. Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988). Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science, 240 (4851):516-518.
56. Marino AP, Dos Santos LI, Henriques PM, et al (2020). Circulating inflammatory mediators as biomarkers of ocular toxoplasmosis in acute and in chronic infection. J Leukoc Biol, 108 (4):1253-1264.
2. Olivera GC, Ross EC, Peuckert C, et al (2021). Blood-brain barrier-restricted translocation of Toxoplasma gondii from cortical capillaries. Elife, 10:e69182.
3. Randall L, Hunter C (2011). Parasite dissemination and the pathogenesis of toxoplasmosis. Eur J Microbiol Immunol (Bp), 1 (1):3-9.
4. Still KM, Batista SJ, O’Brien CA, et al (2020). Astrocytes promote a protective immune response to brain Toxoplasma gondii infection via IL-33-ST2 signaling. PLoS Pathog, 16 (10):e1009027.
5. Melzer T, Cranston H, Weiss L, Halonen S (2010). Host cell preference of Toxoplasma gondii cysts in murine brain: a confocal study. J Neuroparasitology, 1:N100505.
6. Munoz M, Liesenfeld O, Heimesaat MM (2011). Immunology of Toxoplasma gondii. Immunol Rev, 240 (1):269-285.
7. Inagaki M, Aoyama M, Sobue K, et al (2004). Sensitive immunoassays for human and rat GMFB and GMFG, tissue distribution and age-related changes. Biochim Biophys Acta, 1670 (3):208-216.
8. Lim R, Hicklin DJ, Miller JF, et al (1987). Distribution of immunoreactive glia maturation factor-like molecule in organs and tissues. Brain Res, 430(1):93-100.
9. Zaheer A, Zaheer S, Sahu SK, et al (2007). A novel role of glia maturation factor: induction of granulocyte‐macrophage colony‐stimulating factor and pro‐inflammatory cytokines. J Neurochem, 101 (2):364-376.
10. Kempuraj D, Khan MM, Thangavel R, et al (2013). Glia maturation factor induces interleukin-33 release from astrocytes: implications for neurodegenerative diseases. J Neuroimmune Pharmacol, 8 (3):643-650.
11. Fan J, Fong T, Chen X, et al (2018). Glia maturation factor-β: A potential therapeutic target in neurodegeneration and neuroinflammation. Neuropsychiatr Dis Treat, 14:495-504.
12. Luo Y, Zhou Y, Xiao W, et al (2015). Interleukin-33 ameliorates ischemic brain injury in experimental stroke through promoting Th2 response and suppressing Th17 response. Brain Res, 1597:86-94.
13. Yang Y, Liu H, Zhang H, et al (2017). ST2/IL-33-dependent microglial response limits acute ischemic brain injury. J Neurosci, 37 (18):4692-4704.
14. Carlock C, Wu J, Shim J, et al (2017). Interleukin33 deficiency causes tau abnormality and neurodegeneration with Alzheimer-like symptoms in aged mice. Transl Psychiatry, 7 (7):e1164.
15. Fu AK, Hung K-W, Yuen MY, et al (2016). IL-33 ameliorates Alzheimer’s disease-like pathology and cognitive decline. Proc Natl Acad Sci U S A, 113 (19):E2705-E2713.
16. Jiang HR, Milovanović M, Allan D, et al (2012). IL‐33 attenuates EAE by suppressing IL‐17 and IFN‐γ production and inducing alternatively activated macrophages. Eur J Immunol, 42 (7):1804-1814.
17. Li M, Li Y, Liu X, et al (2012). IL-33 blockade suppresses the development of experimental autoimmune encephalomyelitis in C57BL/6 mice. J Neuroimmunol, 247 (1-2):25-31.
18. Jones LA, Roberts F, Nickdel MB, et al (2010). IL‐33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur J Immunol, 40 (2):426-436.
19. Berger O, Li G, Han S-M, et al (2007). Expression of SDF-1 and CXCR4 during reorganization of the postnatal dentate gyrus. Dev Neurosci, 29 (1-2):48-58.
20. Cui L, Qu H, Xiao T, et al (2013). Stromal cell-derived factor-1 and its receptor CXCR4 in adult neurogenesis after cerebral ischemia. Restor Neurol Neurosci, 31 (3):239-251.
21. Tiveron M-C, Cremer H (2008). CXCL12/CXCR4 signalling in neuronal cell migration. Curr Opin Neurobiol, 18 (3):237-244.
22. Kumar P, Lau C, Mathur M, et al (2007). Differential effects of β-arrestins on the internalization, desensitization and ERK1/2 activation downstream of protease activated receptor-2. Am J Physiol Cell Physiol, 293 (1):C346-57.
23. Pujol F, Kitabgi P, Boudin H (2005). The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J Cell Sci, 118 (Pt 5):1071-1080.
24. Safronova A, Araujo A, Camanzo ET, et al (2019). Alarmin S100A11 initiates a chemokine response to the human pathogen Toxoplasma gondii. Nat Immunol, 20 (1):64-72.
25. Foroghi parvar F, Keshavarz H, Shojaee S (2007). Detection of Toxoplasma gondii antigens in sera and urine of experimentally infected mice by capture ELISA. Iran J Parasitol, 3 (1):1-5.
26. Jabari S, Keshavarz H, Salimi M, et al (2018). In vitro culture of Toxoplasma gondii in HeLa, Vero, RBK and A549 cell lines. Infez Med, 26 (2):145-147.
27. Karimi Dermani F, Saidijam M, Amini R, et al (2017). Resveratrol inhibits proliferation, invasion, and epithelial–mesenchymal transition by increasing miR‐200c expression in HCT‐116 colorectal cancer cells. J Cell Biochem, 118 (6):1547-1555.
28. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25 (4):402-408.
29. Santana S, Sastre I, Recuero M, et al (2013). Oxidative stress enhances neurodegeneration markers induced by herpes simplex virus type 1 infection in human neuroblastoma cells. PLoS One, 8 (10):e75842.
30. Pontrello CG, McWhirt JM, Glabe CG, et al (2022). Age-Related Oxidative Redox and Metabolic Changes Precede Intraneuronal Amyloid-β Accumulation and Plaque Deposition in a Transgenic Alzheimer’s Disease Mouse Model. J Alzheimers Dis, 90 (4):1501-1521.
31. Mecocci P, Boccardi V, Cecchetti R, et al (2018). A long journey into aging, brain aging, and Alzheimer’s disease following the oxidative stress tracks. J Alzheimers Dis, 62 (3):1319-1335.
32. Clausen A, Xu X, Bi X, Baudry M (2012). Effects of the superoxide dismutase/catalase mimetic EUK-207 in a mouse model of Alzheimer's disease: protection against and interruption of progression of amyloid and tau pathology and cognitive decline. J Alzheimers Dis, 30 (1):183-208.
33. Zheng C, Zhou M, Sun J, et al (2019). The protective effects of liraglutide on AD-like neurodegeneration induced by oxidative stress in human neuroblastoma SH-SY5Y cells. Chem Biol Interact, 310:108688.
34. Najafi M, Amini R, Maghsood AH, et al (2021). Co expression of GMFβ, IL33, CCL2 and SDF1 genes in the acute stage of toxoplasmosis in mice model and relation for neuronal impairment. Iran J Parasitol, 16 (3):426-434.
35. Zaheer A, Zaheer S, Thangavel R, et al (2008). Glia maturation factor modulates β-amyloid-induced glial activation, inflammatory cytokine/chemokine production and neuronal damage. Brain Res, 1208:192-203.
36. Liu C, Sun W, Zhu T, et al (2022). Glia maturation factor-β induces ferroptosis by impairing chaperone-mediated autophagic degradation of ACSL4 in early diabetic retinopathy. Redox Biol, 52:102292.
37. Selvakumar GP, Iyer SS, Kempuraj D, Ahmed ME, et al (2019). Molecular association of glia maturation factor with the autophagic machinery in rat dopaminergic neurons: a role for endoplasmic reticulum stress and MAPK activation. Mol Neurobiol, 56 (6):3865-3881.
38. Dincel GC, Kul O (2019). First description of enhanced expression of transforming growth factor-alpha (TGF-α) and glia maturation factor-beta (GMF-β) correlate with severity of neuropathology in border disease virus-infected small ruminants. Microb Pathog, 128:301-310.
39. Kumar R, Amruthanjali T, Singothu S, et al (2022). Uncoupling proteins as a therapeutic target for the development of new era drugs against neurodegenerative disorder. Biomed Pharmacother, 147:112656.
40. Thangavel R, Van Hoesen GW, Zaheer A (2009). The abnormally phosphorylated tau lesion of early Alzheimer’s disease. Neurochem Res, 34 (1):118-123.
41. Ramaswamy SB, Bhagavan SM, Kaur H, et al (2019). Glia Maturation Factor in the Pathogenesis of Alzheimer’s disease. Open Access J Neurol Neurosurg, 12 (3):79-82.
42. Luan K, Rosales JL, Lee K-Y (2013). Crosstalks between neurofibrillary tangles and amyloid plaque formation. Ageing Res Rev, 12 (1):174-181.
43. Sun W, Hu C, Wang T, et al (2021). Glia maturation factor beta as a novel biomarker and therapeutic target for hepatocellular carcinoma. Front Oncol, 11:744331.
44. Berrett AN, Gale SD, Erickson LD, et al (2017). Toxoplasma gondii moderates the association between multiple folate-cycle factors and cognitive function in US adults. Nutrients, 9 (6):564.
45. Galeh TM, Ghazvini H, Sarvi S, et al (2022). Controversial Effects of Diverse Types of Toxoplasma gondii on the Anxiety-like Behavior and Cognitive Impairments in the Animal Model of Alzheimer's Disease. Iran J Psychiatry Behav Sci, 16 (3) e122961.
46. Castaño Barrios L, Da Silva Pinheiro AP, Gibaldi D, et al (2021). Behavioral alterations in long-term toxoplasma gondii infection of C57BL/6 mice are associated with neuroinflammation and disruption of the blood brain barrier. PLoS One, 16 (10):e0258199.
47. Wen X, Kudo T, Payne L, et al (2010). Predominant interferon-γ-mediated expression of CXCL9, CXCL10, and CCL5 proteins in the brain during chronic infection with Toxoplasma gondii in BALB/c mice resistant to development of toxoplasmic encephalitis. J Interferon Cytokine Res, 30 (9):653-660.
48. Batista SJ, Still KM, Johanson D, et al (2020). Gasdermin-D-dependent IL-1α release from microglia promotes protective immunity during chronic Toxoplasma gondii infection. Nat Commun, 11 (1):3687.
49. Zhang Y, He J, Zheng H, et al (2019). Association of TREM-1, IL-1β, IL-33/ST2, and TLR expressions with the pathogenesis of ocular toxoplasmosis in mouse models on different genetic backgrounds. Front Microbiol, 10:2264.
50. Liew FY, Pitman NI, McInnes IB (2010). Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol, 10 (2):103-110.
51. Cayrol C (2021). IL-33, an alarmin of the IL-1 family involved in allergic and non allergic inflammation: focus on the mechanisms of regulation of its activity. Cells, 11 (1):107.
52. Ryffel B, Huang F, Robinet P, et al (2019). Blockade of IL-33R/ST2 signaling attenuates Toxoplasma gondii Ileitis depending on IL-22 expression. Front Immunol, 10:702.
53. Ryan N, Anderson K, Volpedo G, et al (2020). The IL-33/ST2 axis in immune responses against parasitic disease: potential therapeutic applications. Front Cell Infect Microbiol, 10:153.
54. de Araújo TE, Coelho-dos-Reis JG, Béla SR, et al (2017). Early serum biomarker networks in infants with distinct retinochoroidal lesion status of congenital toxoplasmosis. Cytokine, 95:102-112.
55. Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988). Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science, 240 (4851):516-518.
56. Marino AP, Dos Santos LI, Henriques PM, et al (2020). Circulating inflammatory mediators as biomarkers of ocular toxoplasmosis in acute and in chronic infection. J Leukoc Biol, 108 (4):1253-1264.
| Files | ||
| Issue | Vol 53 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v53i5.15602 | |
| Keywords | ||
| Toxoplasma gondii Glia maturation factor Interleukin-33 IL33 Chemokine CCL2 Stromal cell derived factor 1 | ||
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How to Cite
1.
Matini M, Amini R, Foroughi-Parvar F. Glia Maturation Factor Beta: A Novel Neuro-Impairment Prediction Factor in Toxoplasmosis. Iran J Public Health. 2024;53(5):1200-1208.
