PlGF knockout delays brain vessel growth and maturation upon systemic hypoxic challenge

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 4, 2012, Pages 663-675

  Freitas Andrade, Moises ^a,b   Carmeliet, Peter ^c,d   Charlebois, Claudie ^a   Stanimirovic, Danica B ^a,b   Moreno, Maria J ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Angiogenesis; brain endothelial cells; hypoxia; pericytes; placental growth factor

Indexed keywords

CLAUDIN 5; FIBRINOGEN; PLACENTAL GROWTH FACTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN BLOOD VESSEL; CELL DISRUPTION; CONTROLLED STUDY; EXTRAVASATION; FIBRINOGEN BLOOD LEVEL; FRONTAL CORTEX; GENOTYPE; HYPOXIA; KNOCKOUT MOUSE; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; WILD TYPE;

ANIMALS; ANOXIA; ASTROCYTES; BRAIN; CEREBROVASCULAR CIRCULATION; CLAUDIN-5; CLAUDINS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEINS; TIGHT JUNCTIONS; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84859427107     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.167     Document Type: Article

References (40)

1. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, Davis RJ, Mizushima N, Rakic P, Dardzinski BJ, Holland SK, Sharp FR, Kuan CY (2006) Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 169:566-83 (Pubitemid 44156315)
2. Adini A, Kornaga T, Firoozbakht F, Benjamin LE (2002) Placental growth factor is a survival factor for tumor endothelial cells and macrophages. Cancer Res 62: 2749-52 (Pubitemid 34525755)
3. Ahmed A, Dunk C, Ahmad S, Khaliq A (2000) Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen-a review. Placenta 21(Suppl A): S16-24
4. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512-23 (Pubitemid 41361741)
5. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C (2010) Pericytes regulate the blood-brain barrier. Nature 468:557-61
6. Autiero M, Luttun A, Tjwa M, Carmeliet P (2003a) Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J Thromb Haemost 1:1356-70
7. Autiero M, Waltenberger J, Communi D, Kranz A, Moons L, Lambrechts D, Kroll J, Plaisance S, De Mol M, Bono F, Kliche S, Fellbrich G, Ballmer-Hofer K, Maglione D, Mayr-Beyrle U, Dewerchin M, Dombrowski S, Stanimirovic D, Van Hummelen P, Dehio C, Hicklin DJ, Persico G, Herbert JM, Communi D, Shibuya M, Collen D, Conway EM, Carmeliet P (2003b) Role of PlGF in the intra-and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med 9:936-43 (Pubitemid 36889938)
8. Beck H, Acker T, Puschel AW, Fujisawa H, Carmeliet P, Plate KH (2002) Cell type-specific expression of neuropilins in an MCA-occlusion model in mice suggests a potential role in post-ischemic brain remodeling. J Neuropathol Exp Neurol 61:339-50 (Pubitemid 34266785)
9. Cao Y, Linden P, Shima D, Browne F, Folkman J (1996) In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor. J Clin Invest 98:2507-11 (Pubitemid 26415071)
10. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7:575-83 (Pubitemid 32448325)
11. Cramer M, Nagy I, Murphy BJ, Gassmann M, Hottiger MO, Georgiev O, Schaffner W (2005) NF-kappaB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells. Biol Chem 386:865-72 (Pubitemid 41448142)
12. del Zoppo GJ (2008) Virchow's triad: the vascular basis of cerebral injury. Rev Neurol Dis 5(Suppl 1): S12-21
13. del Zoppo GJ (2010) The neurovascular unit in the setting of stroke. J Intern Med 267:156-71
14. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores Jr L (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24:909-69
15. Du H, Li P, Pan Y, Li W, Hou J, Chen H, Wang J, Tang H (2010) Vascular endothelial growth factor signaling implicated in neuroprotective effects of placental growth factor in an in vitro ischemic model. Brain Res 1357:1-8
16. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9:669-76 (Pubitemid 36749215)
17. Freitas-Andrade M, Carmeliet P, Stanimirovic DB, Moreno M (2008) VEGFR-2-mediated increased proliferation and survival in response to oxygen and glucose deprivation in PlGF knockout astrocytes. J Neurochem 107:756-67
18. Hamel E (2006) Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100:1059-64 (Pubitemid 43671565)
19. Harik N, Harik SI, Kuo NT, Sakai K, Przybylski RJ, LaManna JC (1996) Time-course and reversibility of the hypoxia-induced alterations in cerebral vascularity and cerebral capillary glucose transporter density. Brain Res 737:335-8 (Pubitemid 26366635)
20. Hayashi T, Noshita N, Sugawara T, Chan PH (2003) Temporal profile of angiogenesis and expression of related genes in the brain after ischemia. J Cereb Blood Flow Metab 23:166-80 (Pubitemid 36188455)
21. Holmes DI, Zachary I (2004) Placental growth factor induces FosB and c-Fos gene expression via Flt-1 receptors. FEBS Lett 557:93-8 (Pubitemid 38115875)
22. Kilic E, Kilic U, Wang Y, Bassetti CL, Marti HH, Hermann DM (2006) The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF0s neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J 20:1185-7
23. Krupinski J, Kaluza J, Kumar P, Kumar S, Wang JM (1994) Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 25:1794-8 (Pubitemid 24274974)
24. Kuo NT, Benhayon D, Przybylski RJ, Martin RJ, LaManna JC (1999) Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain. J Appl Physiol 86:260-4 (Pubitemid 29046965)
25. Kurz H, Fehr J, Nitschke R, Burkhardt H (2008) Pericytes in the mature chorioallantoic membrane capillary plexus contain desmin and alpha-smooth muscle actin: relevance for non-sprouting angiogenesis. Histochem Cell Biol 130:1027-40
26. LaManna JC, Vendel LM, Farrell RM (1992) Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 72:2238-43
27. Liu H, Honmou O, Harada K, Nakamura K, Houkin K, Hamada H, Kocsis JD (2006) Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 129:2734-45 (Pubitemid 44522106)
28. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P (2002) Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8:831-40
29. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG (1991) Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 88:9267-71 (Pubitemid 21915612)
30. Milner R, Hung S, Erokwu B, Dore-Duffy P, LaManna JC, del Zoppo GJ (2008) Increased expression of fibronectin and the alpha5beta1 integrin in angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia. Mol Cell Neurosci 38:43-52
31. Orlidge A, D'Amore PA (1987) Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455-62 (Pubitemid 18029870)
32. Ozerdem U, Stallcup WB (2003) Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6:241-9 (Pubitemid 38506669)
33. Park JE, Chen HH, Winer J, Houck KA, Ferrara N (1994) Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 269:25646-54
34. Sato Y, Rifkin DB (1989) Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 109:309-15 (Pubitemid 19180138)
35. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K (2007) Fibrinogen inhibits neurite outgrowth via beta 3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci USA 104:11814-9 (Pubitemid 47175095)
36. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, Akassoglou K (2010) Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J Neurosci 30:5843-54
37. Takahashi T, Ueno H, Shibuya M (1999) VEGF activates protein kinase C-dependent, but Rasindependent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18: 2221-30 (Pubitemid 29186923)
38. Takeda Y, Uemura S, Iwama H, Imagawa K, Nishida T, Onoue K, Takemoto Y, Soeda T, Okayama S, Somekawa S, Ishigami K, Takaoka M, Kawata H, Kubo A, Horii M, Nakajima T, Saito Y (2009) Treatment with recombinant placental growth factor (PlGF) enhances both angiogenesis and arteriogenesis and improves survival after myocardial infarction. Circ J 73:1674-82
39. Virgintino D, Girolamo F, Errede M, Capobianco C, Robertson D, Stallcup WB, Perris R, Roncali L (2007) An intimate interplay between precocious, migrating pericytes and endothelial cells governs human fetal brain angiogenesis. Angiogenesis 10: 35-45 (Pubitemid 46356222)
40. Ward NL, Moore E, Noon K, Spassil N, Keenan E, Ivanco TL, LaManna JC (2007) Cerebral angiogenic factors, angiogenesis, and physiological response to chronic hypoxia differ among four commonly used mouse strains. J Appl Physiol 102:1927-35 (Pubitemid 46701964)