Complement Peptide C3a Promotes Astrocyte Survival in Response to Ischemic Stress

Molecular Neurobiology

Volumn 53, Issue 5, 2016, Pages 3076-3087

  Shinjyo, Noriko ^a   de Pablo, Yolanda ^a   Pekny, Milos ^a,b,c   Pekna, Marcela ^a,b,c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^c UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Caspase 3; Glial fibrillary acidic protein; Neuroprotection

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; COMPLEMENT COMPONENT C3A; GLIAL FIBRILLARY ACIDIC PROTEIN; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; NERVE GROWTH FACTOR RECEPTOR; VASCULOTROPIN; COMPLEMENT C3A RECEPTOR; COMPLEMENT RECEPTOR; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DEATH; CELL FUNCTION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; GLYCOLYSIS; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; ISCHEMIA; MOLECULAR IMAGING; MOUSE; NEUROPROTECTION; NEWBORN; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; BRAIN ISCHEMIA; C57BL MOUSE; COCULTURE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; INTERMEDIATE FILAMENT; MAPK SIGNALING; METABOLISM; PATHOLOGY; PHENOTYPE; PHYSIOLOGICAL STRESS;

ANIMALS; ASTROCYTES; BRAIN ISCHEMIA; CASPASE 3; CELL SURVIVAL; CEREBRAL CORTEX; COCULTURE TECHNIQUES; COMPLEMENT C3A; ENZYME ACTIVATION; INTERMEDIATE FILAMENTS; MAP KINASE SIGNALING SYSTEM; MICE, INBRED C57BL; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENTS; PHENOTYPE; RECEPTORS, COMPLEMENT; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84929448226     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9204-4     Document Type: Article

References (63)

1. Bélanger M, Magistretti PJ (2009) The role of astroglia in neuroprotection. Dialogues Clin Neurosci 11(3):281–295
2. de Pablo Y, Nilsson M, Pekna M, Pekny M (2013) Intermediate filaments are important for astrocyte response to oxidative stress induced by oxygen-glucose deprivation and reperfusion. Histochem Cell Biol 140(1):81–91
3. Pekny M, Pekna M (2014) Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol Rev 94(4):1077–1098
4. Pekny M, Wilhelmsson U, Pekna M (2014) The dual role of astrocyte activation and reactive gliosis. Neurosci Lett 565:30–38
5. Rossi DJ, Brady JD, Mohr C (2007) Astrocyte metabolism and signaling during brain ischemia. Nat Neurosci 10(11):1377–1386
6. Miklic S, Juric DM, Carman-Krzan M (2004) Differences in the regulation of BDNF and NGF synthesis in cultured neonatal rat astrocytes. Int J Dev Neurosci 22(3):119–130
7. Li L, Lundkvist A, Andersson D, Wilhelmsson U, Nagai N, Pardo AC, Nodin C, Ståhlberg A et al (2008) Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab 28(3):468–481
8. Wilhelmsson U, Li L, Pekna M, Berthold CH, Blom S, Eliasson C, Renner O, Bushong E et al (2004) Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J Neurosci 24(21):5016–5021
9. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME et al (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691–705
10. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK et al (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131(6):1164–1178
11. Berg A, Zelano J, Stephan A, Thams S, Barres BA, Pekny M, Pekna M, Cullheim S (2012) Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3. Exp Neurol 237(1):8–17
12. Perez-Alcazar M, Daborg J, Stokowska A, Wasling P, Björefeldt A, Kalm M, Zetterberg H, Carlström KE et al (2014) Altered cognitive performance and synaptic function in the hippocampus of mice lacking C3. Exp Neurol 253:154–164
13. Rahpeymai Y, Hietala MA, Wilhelmsson U, Fotheringham A, Davies I, Nilsson AK, Zwirner JW RA, Gerard C et al (2006) Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J 25(6):1364–1374
14. Gong B, Pan Y, Zhao W, Knable L, Vempati P, Begum S, Ho L, Wang J et al (2013) IVIG immunotherapy protects against synaptic dysfunction in Alzheimer’s disease through complement anaphylatoxin C5a-mediated AMPA-CREB-C/EBP signaling pathway. Mol Immunol 56(4):619–629
15. Davoust N, Jones J, Stahel PF, Ames RS, Barnum SR (1999) Receptor for the C3a anaphylatoxin is expressed by neurons and glial cells. Glia 26(3):201–211
16. Shinjyo N, Ståhlberg A, Dragonow M, Pekny M, Pekna M (2009) Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells in vitro. Stem Cells 27:2824–2832
17. Järlestedt K, Rousset CI, Ståhlberg A, Sourkova H, Atkins AL, Thornton C, Barnum SR, Wetsel RA et al (2013) Receptor for complement peptide C3a: a therapeutic target for neonatal hypoxic-ischemic brain injury. FASEB J 27(9):3797–3804
18. van Beek J, Bernaudin M, Petit E, Gasque P, Nouvelot A, MacKenzie ET, Fontaine M (2000) Expression of receptors for complement anaphylatoxins C3a and C5a following permanent focal cerebral ischemia in the mouse. Exp Neurol 161(1):373–382
19. Pekny M, Johansson CB, Eliasson C, Stakeberg J, Wallén A, Perlmann T, Lendahl U, Betsholtz C et al (1999) Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol 145(3):503–514
20. Eliasson C, Sahlgren C, Berthold CH, Stakeberg J, Celis JE, Betsholtz C, Eriksson JE, Pekny M (1999) Intermediate filament protein partnership in astrocytes. J Biol Chem 274(34):23996–24006
21. Pekny M, Eliasson C, Chien CL, Kindblom LG, Liem R, Hamberger A, Betsholtz C (1998) GFAP-deficient astrocytes are capable of stellation in vitro when cocultured with neurons and exhibit a reduced amount of intermediate filaments and an increased cell saturation density. Exp Cell Res 239(2):332–343
22. Uliasz TF, Hamby ME, Jackman NA, Hewett JA, Hewett SJ (2012) Generation of primary astrocyte cultures devoid of contaminating microglia. Methods Mol Biol 814:61–79
23. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 1(5):2406–2415
24. Harari OA, Liao JK (2010) NF-kB and innate immunity in ischemic stroke. Ann N Y Acad Sci 1207:32–40
25. Singh N, Sharma G, Mishra V (2012) Hypoxia inducible factor-1: its potential role in cerebral ischemia. Cell Mol Neurobiol 32(4):491–507
26. Hol EM, Pekny M (2015) Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Curr Opin Cell Biol 32:121–130
27. Pekny M, Lane EB (2007) Intermediate filaments and stress. Exp Cell Res 313(10):2244–2254
28. Tokumine J, Kakinohana O, Cizkova D, Smith DW, Marsala M (2003) Changes in spinal GDNF, BDNF, and NT-3 expression after transient spinal cord ischemia in the rat. J Neurosci Res 74(4):552–561
29. Pechan PA, Chowdhury K, Seifert W (1992) Free radicals induce gene expression of NGF and bFGF in rat astrocyte culture. Neuroreport 3(6):469–472
30. van Beek J, Nicole O, Ali C, Ischenko A, MacKenzie ET, Buisson A, Fontaine M (2001) Complement anaphylatoxin C3a is selectively protective against NMDA-induced neuronal cell death. Neuroreport 12(2):289–293
31. Boos L, Szalai AJ, Barnum SR (2005) C3a expressed in the central nervous system protects against LPS-induced shock. Neurosci Lett 387(2):68–71
32. Gürer G, Gursoy-Ozdemir Y, Erdemli E, Can A, Dalkara T (2009) Astrocytes are more resistant to focal cerebral ischemia than neurons and die by a delayed necrosis. Brain Pathol 19(4):630–641
33. Zhuang S, Schnellmann RG (2006) A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 319(3):991–997
34. Sayah S, Jauneau AC, Patte C, Tonon MC, Vaudry H, Fontaine M (2003) Two different transduction pathways are activated by C3a and C5a anaphylatoxins on astrocytes. Brain Res Mol Brain Res 112(1–2):53–60
35. Jauneau AC, Ischenko A, Chan P, Fontaine M (2003) Complement component anaphylatoxins upregulate chemokine expression by human astrocytes. FEBS Lett 537(1–3):17–22
36. Sayah S, Ischenko AM, Zhakhov A, Bonnard AS, Fontaine M (1999) Expression of cytokines by human astrocytomas following stimulation by C3a and C5a anaphylatoxins: specific increase in interleukin-6 mRNA expression. J Neurochem 72(6):2426–2436
37. Jauneau AC, Ischenko A, Chatagner A, Benard M, Chan P, Schouft MT, Patte C, Vaudry H et al (2006) Interleukin-1beta and anaphylatoxins exert a synergistic effect on NGF expression by astrocytes. J Neuroinflammation 3:8
38. Terai K, Matsuo A, McGeer EG, McGeer PL (1996) Enhancement of immunoreactivity for NF-kappa B in human cerebral infarctions. Brain Res 739(1–2):343–349
39. Lian H, Yang L, Cole A, Sun L, Chiang AC, Fowler SW, Shim DJ, Rodriguez-Rivera J et al (2015) NFkB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer’s disease. Neuron 85(1):101–115
40. Martin CB, Ingersoll SA, Martin BK (2007) Transcriptional control of the C3a receptor gene in glial cells: dependence upon AP-1 but not Ets. Mol Immunol 44(5):703–712
41. Michiels C, Minet E, Michel G, Mottet D, Piret JP, Raes M (2001) HIF-1 and AP-1 cooperate to increase gene expression in hypoxia: role of MAP kinases. IUBMB Life 52(1–2):49–53
42. Fujioka S, Niu J, Schmidt C, Sclabas GM, Peng B, Uwagawa T, Li Z, Evans DB et al (2004) NF-κB and AP-1 connection: mechanism of NF-κB-dependent regulation of AP-1 activity. Mol Cell Biol 24(17):7806–7819
43. Fan X, Heijnen CJ, van der Kooij MA, Groenendaal F, van Bel F (2009) The role and regulation of hypoxia-inducible factor-1alpha expression in brain development and neonatal hypoxic-ischemic brain injury. Brain Res Rev 62(1):99–108
44. Jiang BH, Semenza GL, Bauer C, Marti HH (1996) Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 271:C1172–C1180
45. Ebert BJ, Firth JD, Ratcliffe PJ (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences. J Biol Chem 270:29083–29089
46. Heese K, Hock C, Otten U (1998) Inflammatory signals induce neurotrophin expression in human microglial cells. J Neurochem 70(2):699–707
47. Ibáñez CF, Simi A (2012) p75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Trends Neurosci 35(3):431–440
48. Lee TH, Kato H, Chen ST, Kogure K, Itoyama Y (1998) Expression of nerve growth factor and trkA after transient focal cerebral ischemia in rats. Stroke 29(8):1687–1696
49. Rynkowski MA, Kim GH, Garrett MC, Zacharia BE, Otten ML, Sosunov SA, Komotar RJ, Hassid BG et al (2009) C3a receptor antagonist attenuates brain injury after intracerebral hemorrhage. J Cereb Blood Flow Metab 29(1):98–107
50. Ducruet AF, Hassid BG, Mack WJ, Sosunov SA, Otten ML, Fusco DJ, Hickman ZL, Kim GH et al (2008) C3a receptor modulation of granulocyte infiltration after murine focal cerebral ischemia is reperfusion dependent. J Cereb Blood Flow Metab 28(5):1048–1058
51. Ducruet AF, Zacharia BE, Sosunov SA, Gigante PR, Yeh ML, Gorski JW, Otten ML, Hwang RY et al (2012) Complement inhibition promotes endogenous neurogenesis and sustained anti-inflammatory neuroprotection following reperfused stroke. PLoS One 7(6):e38664
52. Mathieu MC, Sawyer N, Greig GM, Hamel M, Kargman S, Ducharme Y, Lau CK, Friesen RW et al (2005) The C3a receptor antagonist SB 290157 has agonist activity. Immunol Lett 100(2):139–145
53. Liu Z, Li Y, Cui Y, Roberts C, Lu M, Wilhelmsson U, Pekny M, Chopp M (2014) Beneficial effects of GFAP/Vimentin reactive astrocytes for axonal remodeling and motor behavioral recovery in mice after stroke. Glia 62(12):2022–2033
54. Ding M, Eliasson C, Betsholtz C, Hamberger A, Pekny M (1998) Altered taurine release following hypotonic stress in astrocytes from mice deficient for GFAP and vimentin. Brain Res Mol Brain Res 62(1):77–81
55. Menet V, Prieto M, Privat A, Giménez Y, Ribotta M (2003) Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci U S A 100(15):8999–9004
56. Cho KS, Yang L, Lu B, Feng Ma H, Huang X, Pekny M, Chen DF (2005) Re-establishing the regenerative potential of central nervous system axons in postnatal mice. J Cell Sci 118(Pt 5):863–872
57. Kinouchi R, Takeda M, Yang L, Wilhelmsson U, Lundkvist A, Pekny M, Chen DF (2003) Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat Neurosci 6(8):863–868
58. Widestrand A, Faijerson J, Wilhelmsson U, Smith PL, Li L, Sihlbom C, Eriksson PS, Pekny M (2007) Increased neurogenesis and astrogenesis from neural progenitor cells grafted in the hippocampus of GFAP−/− Vim−/− mice. Stem Cells 25(10):2619–2627
59. Larsson A, Wilhelmsson U, Pekna M, Pekny M (2004) Increased cell proliferation and neurogenesis in the hippocampal dentate gyrus of old GFAP (−/−) Vim (−/−) mice. Neurochem Res 29(11):2069–2073
60. Wilhelmsson U, Faiz M, de Pablo Y, Sjöqvist M, Andersson D, Widestrand A, Potokar M, Stenovec M et al (2012) Astrocytes negatively regulate neurogenesis through the JAGGED1-mediated notch pathway. Stem Cells 30(10):2320–2329
61. Järlestedt K, Rousset CI, Faiz M, Wilhelmsson U, Ståhlberg A, Sourkova H, Pekna M, Mallard C et al (2010) Attenuation of reactive gliosis does not affect infarct volume in neonatal hypoxic-ischemic brain injury in mice. PLoS One 5(4):e10397
62. Yeo S, Bandyopadhyay S, Messing A, Brenner M (2013) Transgenic analysis of GFAP promoter elements. Glia 61(9):1488–1499
63. Nakazawa T, Takeda M, Lewis GP, Cho KS, Jiao J, Wilhelmsson U, Fisher SK, Pekny M et al (2007) Attenuated glial reactions and photoreceptor degeneration after retinal detachment in mice deficient in glial fibrillary acidic protein and vimentin. Invest Ophthalmol Vis Sci 48(6):2760–2768