Perlecan domain V modulates astrogliosis In vitro and after focal cerebral ischemia through multiple receptors and increased nerve growth factor release

GLIA

Volumn 59, Issue 12, 2011, Pages 1822-1840

  Al Ahmad, Abraham J ^a   Lee, Boyeon ^a   Saini, Maxim ^a   Bix, Gregory J ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Alpha dystroglycan; Astrocytes; Astrogliosis; Nerve growth factor; Perlecan domain V

Indexed keywords

ALPHA DYSTROGLYCAN; GELATINASE A; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMAN RECOMBINANT PERLECAN DOMAIN V; ILOMASTAT; INTEGRIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; NEUROCAN; NEUROPROTECTIVE AGENT; PERLECAN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN ISCHEMIA; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECRETION; RAT; SCAR FORMATION;

ANIMALS; ASTROCYTES; BRAIN INFARCTION; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; GLIOSIS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MALE; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; PEPTIDE FRAGMENTS; PRIMARY CELL CULTURE; PROTEIN STRUCTURE, TERTIARY; RATS; UP-REGULATION;

EID: 80053561988     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21227     Document Type: Article

References (38)

1. Aga M, Bradley JM, Keller KE, Kelley MJ, Acott TS. 2008. Specialized podosome- or invadopodia-like structures (PILS) for focal trabecular meshwork extracellular matrix turnover. Invest Ophthalmol Vis Sci 49: 5353-5365.
2. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, Opdenakker G, Sorokin LM. 2006. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203: 1007-1019.
3. Al Ahmad A, Lee B, Stack J, Parham C, Campbell J, Clarke D, Fertala A, Bix GJ. 2010. Endostatin binds nerve growth factor and thereby inhibits neurite outgrowth and neuronal migration in-vitro. Brain Res 1360: 28-39.
4. Aronowski J, Grotta JC, Strong R, Waxham MN. 2000. Interplay between the gamma isoform of PKC, calcineurin in regulation of vulnerability to focal cerebral ischemia. J Cereb Blood Flow Metab 20: 343-349.
5. Baronas-Lowell D, Lauer-Fields JL, Fields GB. 2004. Induction of endothelial cell activation by a triple helical alpha2beta integrin ligand, derived from type I collagen alpha1(I)496-507. J Biol Chem 279: 952-962.
6. Bix G, Fu J, Gonzalez EM, Macro L, Barker A, Campbell S, Zutter MM, Santoro SA, Kim JK, Höök M, Reed CC, Iozzo RV. 2004. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J Cell Biol 166: 97-109.
7. Bix G, Iozzo RA, Woodall B, Burrows M, McQuillan A, Campbell S, Fields GB, Iozzo RV. 2007. Endorepellin, the C-terminal angiostatic module of perlecan, enhances collagen-platelet responses via the alpha2beta1-integrin receptor. Blood 109: 3745-3748.
8. Block MR, Badowski C, Millon-Fremillon A, Bouvard D, Bouin AP, Faurobert E, Gerber-Scokaert D, Planus E, Albiges-Rizo C. 2008. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur J Cell Biol 87: 491-506.
9. Booher J, Sensenbrenner M. 1972. Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask cultures. Neurobiology 2: 97-105.
10. Bozzi M, Inzitari R, Sbardell D, Monaco S, Pavoni E, Gioia M, Marini S, Morlacchi S, Sciandra F, Castagnola M, Giardina B, Brancaccio A, Coletta M. 2009. Enzymatic processing of beta-dystroglycan recombinant ectodomain by MMP-9: Identification of the main cleavage site. IUBMB Life 61: 1143-1152.
11. Cirillo G, Bianco MR, Colangelo AM, Cavaliere C, Daniele DL, Zaccaro L, Alberghina L, Papa M. 2010. Reactive astrocytosis-induced perturbation of synaptic homeostasis is restored by nerve growth factor. Neurobiol Dis 41: 630-639.
12. Cragnolini AB, Huang Y, Gokina P, Friedman WJ. 2009. Nerve growth factor attenuates proliferation of astrocytes via the p75 neurotrophin receptor. Glia 57: 1386-1392.
13. Hamby ME, Sofroniew MV. 2010. Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7: 494-506.
14. Kikkawa Y, Yu H, Genersch E, Sanzen N, Sekiguchi K, Fassler R, Campbell KP, Talts JF, Ekblom P. 2004. Laminin isoforms differentially regulate adhesion, spreading, proliferation, and ERK activation of beta1 integrin-null cells. Exp Cell Res 300: 94-108.
15. Lee B, Clarke D, Al Ahmad A, Kahle M, Parham C, Auckland L, Shaw C, FIdanboylu M, Orr AW, Ogunshola OO, Fertala A, Thomas SA, Bix GJ. 2011. Perlecan domain V. Perlecan domain V is neuroprotective and pro-angiogenic following ischemic brain stroke in mice and rats. J Clin Invest [Epub ahead of print].
16. 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: 1687-1696; discussion 1697.
17. Linder S. 2007. The matrix corroded: Podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17: 107-117.
18. Milner R, Hung S, Wang X, Spatz M, del Zoppo GJ. 2008. The rapid decrease in astrocyte-associated dystroglycan expression by focal cerebral ischemia is protease-dependent. J Cereb Blood Flow Metab 28: 812-823.
19. Mongiat M, Sweeney SM, San Antonio JD, Fu J, Iozzo RV. 2003. Endorepellin, a novel inhibitor of angiogenesis derived from the C terminus of perlecan. J Biol Chem 278: 4238-4249.
20. Nystrom A, Shaik ZP, Gullberg D, Krieg T, Eckes B, Zent R, Pozzi A, Iozzo RV. 2009. Role of tyrosine phosphatase SHP-1 in the mechanism of endorepellin angiostatic activity. Blood 114: 4897-4906.
21. Pacifici R, Basilico C, Roman J, Zutter MM, Santoro SA, McCracken R. 1992. Collagen-induced release of interleukin 1 from human blood mononuclear cells. Potentiation by fibronectin binding to the alpha 5 beta 1 integrin. J Clin Invest 89: 61-67.
22. Rolls A, Shechter R, Schwartz M. 2009. The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10: 235-241.
23. Schmid-Brunclik N, Burgi-Taboada C, Antoniou X, Gassmann M, Ogunshola OO. 2008. Astrocyte responses to injury: VEGF simultaneously modulates cell death and proliferation. Am J Physiol Regul Integr Comp Physiol 295: R864-R873.
24. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647.
25. Sofroniew MV, Vinters HV. 2010. Astrocytes: Biology and pathology. Acta Neuropathol 119: 7-35.
26. Spence HJ, Dhillon AS, James M, Winder SJ. 2004. Dystroglycan, a scaffold for the ERK-MAP kinase cascade. EMBO Rep 5: 484-489.
27. Sweeney SM, DiLullo G, Slater SJ, Martinez J, Iozzo RV, Lauer-Fields JL, Fields GB, San Antonio JD. 2003. Angiogenesis in collagen I requires alpha2beta1 ligation of a GFP*GER sequence and possibly p38 MAPK activation and focal adhesion disassembly. J Biol Chem 278: 30516-30524.
28. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 1999. Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J 18: 863-870.
29. Thompson O, Kleino I, Crimaldi L, Gimona M, Saksela K, Winder SJ. 2008. Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS One 3: e3638.
30. Waxham MN, Grotta JC, Silva AJ, Strong R, Aronowski J. 1996. Ischemia-induced neuronal damage: A role for calcium/calmodulin-dependent protein kinase II. J Cereb Blood Flow Metab 16: 1-6.
31. Wijelath ES, Rahman S, Murray J, Patel Y, Savidge G, Sobel M. 2004. Fibronectin promotes VEGF-induced CD34 cell differentiation into endothelial cells. J Vasc Surg 39: 655-660.
32. Wolburg-Buchholz K, Mack AF, Steiner E, Pfeiffer F, Engelhardt B, Wolburg H. 2009. Loss of astrocyte polarity marks blood-brain barrier impairment during experimental autoimmune encephalomyelitis. Acta Neuropathol 118: 219-233.
33. Wright S, Parham C, Lee B, Clarke D, Auckland L, Johnston J, Lawrence AL, Dickeson SK, Santoro SA, Griswold-Prenner I, Bix GJ. 2010. Perlecan domain V inhibits alpha2 integrin-mediated amyloid-beta neurotoxicity. Neurobiol Aging [Epub ahead of print].
34. Wu VW, Nishiyama N, Schwartz JP. 1998. A culture model of reactive astrocytes: Increased nerve growth factor synthesis and reexpression of cytokine responsiveness. J Neurochem 71: 749-756.
35. Xiao H, Bai XH, Kapus A, Lu WY, Mak AS, Liu M. 2010. The protein kinase C cascade regulates recruitment of matrix metalloprotease 9 to podosomes and its release and activation. Mol Cell Biol 30: 5545-5561.
36. Zhong D, Saito F, Saito Y, Nakamura A, Shimizu T, Matsumura K. 2006. Characterization of the protease activity that cleaves the extracellular domain of beta-dystroglycan. Biochem Biophys Res Commun 345: 867-871.
37. Zhu W, Cheng S, Xu G, Ma M, Zhou Z, Liu D, Liu X. 2011. Intranasal nerve growth factor enhances striatal neurogenesis in adult rats with focal cerebral ischemia. Drug Deliv 18: 338-343.
38. Zimmermann DR, Dours-Zimmermann MT. 2008. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130: 635-653.