STAT3-Mediated astrogliosis protects myelin development in neonatal brain injury

Annals of Neurology

Volumn 72, Issue 5, 2012, Pages 750-765

  Nobuta, Hiroko ^a,b   Ghiani, Cristina A ^a   Paez, Pablo M ^a   Spreuer, Vilma ^a   Dong, Hongmei ^a   Korsak, Rose A ^a   Manukyan, Armine ^a   Li, Jiaxi ^a   Vinters, Harry V ^b   Huang, Eric J ^c,d   Rowitch, David H ^d   Sofroniew, Michael V ^a   Campagnoni, Anthony T ^a   De Vellis, Jean ^a   Waschek, James A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; MYELIN; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CADAVER; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DOSE RESPONSE; GENE DELETION; GENETIC ENGINEERING; HUMAN; HUMAN TISSUE; MOLECULAR MECHANICS; MOUSE; NERVE CELL CULTURE; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WHITE MATTER INJURY; WILD TYPE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BENZAMIDES; BRAIN INJURIES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; DIOXOLES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HUMANS; INFANT; INFANT, NEWBORN; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN SHEATH; POSTMORTEM CHANGES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; STAT3 TRANSCRIPTION FACTOR; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84871971523     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23670     Document Type: Article

References (62)

1. Back SA,. Perinatal white matter injury: The changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev 2006; 12: 129-140.
2. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA,. Reprint of "The developing oligodendrocyte: key cellular target in brain injury in the premature infant." Int J Dev Neurosci 2011; 29: 565-582.
3. Silbereis JC, Huang EJ, Back SA, Rowitch DH,. Towards improved animal models of neonatal white matter injury associated with cerebral palsy. Dis Model Mech 2010; 3: 678-688.
4. Dyet LE, Kennea N, Counsell SJ, et al. Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 2006; 118: 536-548. (Pubitemid 46085408)
5. Rezaie P, Dean A,. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 2002; 22: 106-132. (Pubitemid 35252702)
6. Blumenthal I,. Periventricular leucomalacia: A review. Eur J Pediatr 2004; 163: 435-442. (Pubitemid 39013114)
7. Deng W, Pleasure J, Pleasure D,. Progress in periventricular leukomalacia. Arch Neurol 2008; 65: 1291-1295.
8. Bhutta AT, Cleves MA, Casey PH, et al. Cognitive and behavioral outcomes of school-aged children who were born preterm: A meta-analysis. JAMA 2002; 288: 728-737. (Pubitemid 34848226)
9. Constable RT, Ment LR, Vohr BR, et al. Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: An investigation of group and gender effects. Pediatrics 2008; 121: 306-316. (Pubitemid 351198453)
10. Skranes J, Vangberg TR, Kulseng S, et al. Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 2007; 130: 654-666. (Pubitemid 46410747)
11. Dammann O, Leviton A,. Inflammatory brain damage in preterm newborns-dry numbers, wet lab, and causal inferences. Early Hum Dev 2004; 79: 1-15. (Pubitemid 39036744)
12. Leviton A, Paneth N, Reuss ML, et al. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Developmental Epidemiology Network Investigators. Pediatr Res 1999; 46: 566-575. (Pubitemid 29496486)
13. Chau V, Brant R, Poskitt KJ, et al. Postnatal infection is associated with widespread abnormalities of brain development in premature newborns. Pediatr Res 2012; 71: 274-279.
14. Nelson KB, Grether JK, Dambrosia JM, et al. Neonatal cytokines and cerebral palsy in very preterm infants. Pediatr Res 2003; 53: 600-607. (Pubitemid 36406730)
15. Wu YW,. Systematic review of chorioamnionitis and cerebral palsy. Ment Retard Dev Disabil Res Rev 2002; 8: 25-29. (Pubitemid 34754490)
16. Yoon BH, Romero R, Yang SH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996; 174: 1433-1440. (Pubitemid 26165257)
17. Roessmann U, Gambetti P,. Pathological reaction of astrocytes in perinatal brain injury. Immunohistochemical study. Acta Neuropathol 1986; 70: 302-307. (Pubitemid 16046833)
18. Hirayama A, Okoshi Y, Hachiya Y, et al. Early immunohistochemical detection of axonal damage and glial activation in extremely immature brains with periventricular leukomalacia. Clin Neuropathol 2001; 20: 87-91. (Pubitemid 32234490)
19. Deguchi K, Oguchi K, Takashima S,. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol 1997; 16: 296-300. (Pubitemid 27329934)
20. Andiman SE, Haynes RL, Trachtenberg FL, et al. The cerebral cortex overlying periventricular leukomalacia: Analysis of pyramidal neurons. Brain Pathol 2010; 20: 803-814.
21. Sofroniew MV, Vinters HV,. Astrocytes: biology and pathology. Acta Neuropathol 2010; 119: 7-35.
22. Billiards SS, Haynes RL, Folkerth RD, et al. Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 2008; 18: 153-163. (Pubitemid 351430393)
23. Buser JR, Maire J, Riddle A, et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012; 71: 93-109.
24. Herrmann JE, Imura T, Song B, et al. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 2008; 28: 7231-7243.
25. Garcia AD, Doan NB, Imura T, et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004; 7: 1233-1241. (Pubitemid 39426243)
26. Takeda K, Kaisho T, Yoshida N, et al. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol 1998; 161: 4652-4660. (Pubitemid 28492039)
27. Soriano P,. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21: 70-71. (Pubitemid 29036285)
28. Amur-Umarjee S, Phan T, Campagnoni AT,. Myelin basic protein mRNA translocation in oligodendrocytes is inhibited by astrocytes in vitro. J Neurosci Res 1993; 36: 99-110. (Pubitemid 23260466)
29. Suzumura A, Bhat S, Eccleston PA, et al. The isolation and long-term culture of oligodendrocytes from newborn mouse brain. Brain Res 1984; 324: 379-383. (Pubitemid 15195977)
30. Agresti C, D'Urso D, Levi G,. Reversible inhibitory effects of interferon-gamma and tumour necrosis factor-alpha on oligodendroglial lineage cell proliferation and differentiation in vitro. Eur J Neurosci 1996; 8: 1106-1116. (Pubitemid 26174637)
31. Yoshida T, Takeuchi M,. Primary culture and cryopreservation of mouse astrocytes under serum-free conditions. Cytotechnology 1991; 5: 99-106.
32. Michler-Stuke A, Wolff J, Bottenstein JE,. Factors influencing astrocyte growth and development in defined media. Int J Dev Neurosci 1984; 2: 575-584.
33. Haynes RL, Folkerth RD, Keefe RJ, et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 2003; 62: 441-450. (Pubitemid 36560186)
34. Sofroniew MV,. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009; 32: 638-647.
35. Volpe JJ,. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001; 50: 553-562. (Pubitemid 33009976)
36. Back SA, Riddle A, McClure MM,. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007; 38: 724-730. (Pubitemid 46184249)
37. Craig A, Ling Luo N, Beardsley DJ, et al. Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol 2003; 181: 231-240. (Pubitemid 36629244)
38. Hasegawa M, Houdou S, Mito T, et al. Development of myelination in the human fetal and infant cerebrum: A myelin basic protein immunohistochemical study. Brain Dev 1992; 14: 1-6.
39. Hagberg H, Peebles D, Mallard C,. Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 2002; 8: 30-38. (Pubitemid 34754491)
40. Choi EK, Park D, Kim TK, et al. Animal models of periventricular leukomalacia. Lab Anim Res 2011; 27: 77-84.
41. Ferriero DM, Miller SP,. Imaging selective vulnerability in the developing nervous system. J Anat 2010; 217: 429-435.
42. Skranes J, Vangberg TR, Kulseng S, et al. Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 2007; 130: 654-666. (Pubitemid 46410747)
43. Nguyen The Tich S, Anderson PJ, Shimony JS, et al. A novel quantitative simple brain metric using MR imaging for preterm infants. AJNR Am J Neuroradiol 2009; 30: 125-131.
44. Fu J, Xue X, Chen L, et al. Studies on the value of diffusion-weighted MR imaging in the early prediction of periventricular leukomalacia. J Neuroimaging 2009; 19: 13-18.
45. Nagy Z, Jonsson B,. Cerebral MRI findings in a cohort of ex-preterm and control adolescents. Acta Paediatr 2009; 98: 996-1001.
46. Sofroniew MV,. Transgenic techniques for cell ablation or molecular deletion to investigate functions of astrocytes and other GFAP-expressing cell types. Methods Mol Biol 2012; 814: 531-544.
47. Menn B, Garcia-Verdugo JM, Yaschine C, et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006; 26: 7907-7918. (Pubitemid 44315160)
48. Pietenpol JA, Stein RW, Moran E, et al. TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 1990; 61: 777-785.
49. Defacque H, Piquemal D, Basset A, et al. Transforming growth factor-beta1 is an autocrine mediator of U937 cell growth arrest and differentiation induced by vitamin D3 and retinoids. J Cell Physiol 1999; 178: 109-119. (Pubitemid 28554929)
50. Yang X, Chen L, Xu X, et al. TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 2001; 153: 35-46. (Pubitemid 34280192)
51. Marone M, Scambia G, Bonanno G, et al. Transforming growth factor-beta1 transcriptionally activates CD34 and prevents induced differentiation of TF-1 cells in the absence of any cell-cycle effects. Leukemia 2002; 16: 94-105. (Pubitemid 34105604)
52. Sarafian TA, Montes C, Imura T, et al. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 2010; 5: e9532.
53. Inman GJ, Nicolas FJ, Callahan JF, et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2002; 62: 65-74. (Pubitemid 34680517)
54. Ronaldson PT, Demarco KM, Sanchez-Covarrubias L, et al. Transforming growth factor-beta signaling alters substrate permeability and tight junction protein expression at the blood-brain barrier during inflammatory pain. J Cereb Blood Flow Metab 2009; 29: 1084-1098.
55. Waghabi MC, de Souza EM, de Oliveira GM, et al. Pharmacological inhibition of transforming growth factor beta signaling decreases infection and prevents heart damage in acute Chagas' disease. Antimicrob Agents Chemother 2009; 53: 4694-4701.
56. Lonardo E, Hermann PC, Mueller MT, et al. Nodal/Activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 2011; 9: 433-446.
57. De Groot CJ, Montagne L, Barten AD, et al. Expression of transforming growth factor (TGF)-beta1, -beta2, and -beta3 isoforms and TGF-beta type I and type II receptors in multiple sclerosis lesions and human adult astrocyte cultures. J Neuropathol Exp Neurol 1999; 58: 174-187. (Pubitemid 29088941)
58. Zhang Y, Zhang J, Navrazhina K, et al. TGFbeta1 induces Jagged1 expression in astrocytes via ALK5 and Smad3 and regulates the balance between oligodendrocyte progenitor proliferation and differentiation. Glia 2010; 58: 964-974.
59. Ishibashi T, Dakin KA, Stevens B, et al. Astrocytes promote myelination in response to electrical impulses. Neuron 2006; 49: 823-832. (Pubitemid 43376080)
60. Albrecht PJ, Murtie JC, Ness JK, et al. Astrocytes produce CNTF during the remyelination phase of viral-induced spinal cord demyelination to stimulate FGF-2 production. Neurobiol Dis 2003; 13: 89-101. (Pubitemid 36793975)
61. Messersmith DJ, Murtie JC, Le TQ, et al. Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J Neurosci Res 2000; 62: 241-256.
62. Back SA, Tuohy TM, Chen H, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med 2005; 11: 966-972. (Pubitemid 41294442)