Contraindications of VEGF-based therapeutic angiogenesis: Effects on macrophage density and histology of normal and ischemic brains

Vascular Pharmacology

Volumn 44, Issue 5, 2006, Pages 316-325

  Manoonkitiwongsa, Panya S ^a   Schultz, Robert L ^b   Whitter, Ernest F ^b   Lyden, Patrick D ^c  

^a Institutes   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Angiogenesis; Macrophages; Neuroprotection; Stroke; Vascular endothelial growth factor

Indexed keywords

VASCULOTROPIN 165;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN ISCHEMIA; CELL COUNT; CELL DENSITY; CELL INFILTRATION; CONTROLLED STUDY; CORRELATION ANALYSIS; HISTOLOGY; MACROPHAGE; MALE; MONOTHERAPY; NERVOUS TISSUE; NEUROPROTECTION; NEUTROPHIL; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT; TREATMENT CONTRAINDICATION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; INFARCTION, MIDDLE CEREBRAL ARTERY; INFUSION PUMPS, IMPLANTABLE; MACROPHAGES; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROPIL; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33646142053     PISSN: 15371891     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vph.2006.01.008     Document Type: Article

References (61)

1. Al-Khaldi A., Eliopoulos N., Martineau D., Lejeune L., Lachapelle K., and Galipeau J. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther. 10 (2003) 621-629
2. Alvarez J.A., Baird A., Tatum A., Daucher J., Chorsky R., Gonzalez A.M., and Stopa E.G. Localization of basic fibroblast growth factor and vascular endothelial growth factor in human glial neoplasms. Mod. Path. 5 (1992) 303-307
3. Bates D.O., and Harper S.J. Regulation of vascular permeability by vascular endothelial growth factors. Vascul. Pharmacol. 39 (2002) 225-237
4. Bates D.O., Hillman N.J., Williams B., Neal C.R., and Pocock T.M. Regulation of microvascular permeability by vascular endothelial growth factors. J. Anat. 200 (2002) 581-597
5. Bederson J.B., Pitts L.H., Tsuji M., Nishimura M.C., Davis R.L., and Bartowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17 (1986) 472-476
6. Bellomo M., Adamo E.B., Deodato B., Catania M.A., Mannucci C., Marini H., Marciano M.C., Marini R., Sapienza S., Giacca M., Caputi A.P., Squadrito F., and Calapai G. Enhancement of expression of vascular endothelial growth factor after adeno-associated virus gene transfer is associated with improvement of brain ischemia injury in the gerbil. Pharmacol. Res. 48 (2003) 309-317
7. Bian X.W., Du L.L., Shi J.Q., Cheng Y.S., and Liu F.X. Correlation of bFGF, FGFR-1 and VEGF expression with vascularity and malignancy of human astrocytomas. Anal. Quant. Cytol. Histol. 22 (2000) 267-274
8. Bogousslavsky J., Victor S.J., Salinas E.O., Pallay A., Donnan G.A., Fieschi C., Kaste M., Orgogonzo J.M., Chamorro A., and Desmet A. Fiblast (trafermin) in acute stroke: results of the European-Australian phase II/III safety and efficacy trial. Cerebrovasc. Dis. 14 (2002) 239-251
9. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., and During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36 (2004) 827-835
10. Carmeliet P., and Storkebaum E. Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin. Cell Dev. Biol. 13 (2002) 39-53
11. Chen J., Zhang C., Jiang H., Li Y., Zhang L., Robin A., Katakowski M., Lu M., and Chopp M. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J. Cereb. Blood Flow Metab. 25 (2005) 281-290
12. Cheng Y.D., Al-Khoury L., and Zivin J.A. Neuroprotection for ischemic stroke: two decades of success and failure. J. Am. Soc. Exp. Neurotherapeutics 1 (2004) 36-45
13. Chong Z.Z., Kang J.Q., and Maiese K. Angiogenesis and plasticity: role of erythropoietin in vascular systems. J. Hematother. Stem Cell Res. 11 (2002) 863-871
14. Croll S.D., Goodman J.H., and Scharfman H.E. Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. Adv. Exp. Med. Biol. 548 (2004) 57-68
15. Croll S.D., Ransohoff R.M., Cai N., Zhang Q., Martin F.J., Wei T., Kasselman L.J., Kintner J., Murphy A.J., Yancopoulos G.D., and Weigand S.I. VEGF-mediated inflammation precedes angiogenesis in adult brain. Exp. Neurol. 187 (2004) 388-402
16. D'Angelo G., Lee H., and Weiner R.I. cAMP-dependent protein kinase inhibits the mitogenic action of vascular endothelial growth factor and fibroblast growth factor in capillary endothelial cells by blocking Raf activation. J. Cell. Biochem. 1 (1997) 353-366
17. Dobrogowska D.H., Lossinsky A.S., Tarnawski M., and Vorbrodt A.W. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J. Neurocytol. 27 (1998) 163-173
18. Ehrenreich H., Hasselblatt M., Dembowski C., Cepek L., Lewczuk P., Stiefel M., Rustenbeck H.H., Breiter N., Jacob S., Knerlich F., Bohn M., Poser W., Ruther E., Kochen M., Gefeller O., Gleiter C., Wessel T.C., De Ryck M., Itri L., Prange H., Cerami A., Brines M., and Siren A.L. Erythropoietin therapy for acute stroke is safe and beneficial. Mol. Med. 8 (2002) 495-505
19. Ferrara N. Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: therapeutic implications. Semin. Oncol. 29 (2002) 10-14
20. Ferrara N., and Gerber H.P. The role of vascular endothelial growth factor in angiogenesis. Acta Haematol. 106 (2001) 148-156
21. Forstreuter F., Lucius R., and Mentlein R. Vascular endothelial growth factor induces chemotaxis and proliferation of microglial cells. J. Neuroimmunol. 1323 (2002) 93-98
22. Greenberg D.A. Angiogenesis and stroke. Drug News Perspect. 11 (1998) 265-270
23. Greenberg D.A., and Jin K. VEGF and ALS: the luckiest growth factor?. Trends Mol. Med. 10 (2004) 1-3
24. Heil M., Clauss M., Suzuki K., Buschmann I.R., Willuweit A., Fischer S., and Schaper W. Vascular endothelial growth factor (VEGF) stimulates monocyte migration through endothelial monolayers via increased integrin expression. Eur. J. Cell Biol. 79 (2000) 850-857
25. Isner J.M. Vascular endothelial growth factor: gene therapy and therapeutic angiogenesis. Am. J. Cardiol. 82 (1998) 63S-64S
26. Isner J.M., Pieczek A., Schainfeld R., Blair R., Haley L., Asahara T., Rosenfield K., Rasvi S., Walsh K., and Symes J.F. Clinical evidence of angiogenesis after arterial gene transfer of ph VEGF165 in patient with ischaemic limb. Lancet 348 (1996) 370-374
27. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., and Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. 99 (2002) 11946-11950
28. Kanda S., Miyata Y., and Kanetake H. Fibroblast growth factor-2-mediated capillary morphogenesis of endothelial cells requires signals via Flt-1/vascular endothelial growth factor receptor-1: possible involvement of c-Akt. J. Biol. Chem. 297 (2004) 4007-4016
29. Kaya D., Gursoy-Ozdemir Y., Yemisci M., Tuncer N., Sevinc A., and Dalkara T. VEGF protects brain against focal ischemia without increasing blood-brain permeability when administered intracerebroventricularly. J. Cereb. Blood Flow Metab. 25 (2005) 1111-1118
30. Kim J.H., Chung Y.G., Kim C.Y., Kim H.K., and Lee H.K. Upregulation of VEGF and FGF2 in normal rat brain after experimental intraoperative radiation therapy. J. Korean Med. Sci. 19 (2004) 879-886
31. Kinnaird T., Stabile E., Burnett M.S., and Epstein S.E. Bone-marrow-derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences. Circ. Res. 95 (2004) 354-363
32. Krupinski J., Stroemer P., Slevin M., Marti E., Kumar P., and Rubio F. Three-dimensional structure and survival of newly formed blood vessels after focal cerebral ischemia. NeuroReport 14 (2003) 1171-1176
33. Li F., Chong Z.Z., and Maiese K. Erythropoietin on a tightrope: balancing neuronal and vascular protection between intrinsic and extrinsic pathways. NeuroSignals 13 (2004) 265-289
34. Longa E.Z., Weinstein P.R., Carlson S., and Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20 (1989) 84-91
35. Losordo D.W., Vale P.R., Symes J.F., Dunnington C.H., Esakof D.D., Maysky M., Ashare A.B., Lahti K., and Isner J.M. Gene therapy for myocardial angiogenesis: initial clinical results with direct myocardial injection of ph VEGF165 as sole therapy for myocardial ischemia. Circulation 98 (1998) 2800-2804
36. Malaguarnera L., Imbesi R.M., Scuto A., D'Amico F., Licata F., Messina A., and Sanfilippo S. Prolactin increases HO-1 expression and induces VEGF production in human macrophages. J. Cell. Biochem. 93 (2004) 197-206
37. Manoonkitiwongsa P.S., Jackson-Friedman C., McMillan P.J., Schultz R.L., and Lyden P.D. Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J. Cereb. Blood Flow Metab. 21 (2001) 1223-1231
38. Manoonkitiwongsa P.S., Schultz R.L., McCreery D.B., Whitter E.F., and Lyden P.D. Neuroprotection of ischemic brain by vascular endothelial growth factor is critically dependent on proper dosage and may be compromised by angiogenesis. J. Cereb. Blood Flow Metab. 24 (2004) 693-702
39. Marti H.H. Erythropoietin and the hypoxic brain. J. Exp. Biol. 207 (2004) 233-242
40. Moore M.A., Hattori K., Heissig B., Shieh J.H., Dias S., Crystal R.G., and Rafii S. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann. N.Y. Acad. Sci. 938 (2001) 36-45
41. Persson L., Hardemark H.G., Bolander H.G., Hillered L., and Olsson Y. Neurologic and neuropathologic outcome after middle cerebral artery occlusion in rats. Stroke 20 (1989) 641-645
42. Pettersson A., Nagy J.A., Brown L.F., Sundberg C., Morgan E., Jungles S., Carter R., Krieger J.E., Manseau E.J., Harvey V.S., Eckelhoefer I.A., Feng D., Dvorak A.M., Mulligan R.C., and Dvorak H.F. Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80 (2000) 99-115
43. Plate K.H. Mechanisms of angiogenesis in the brain. J. Neuropathol. Exp. Neurol. 58 (1999) 313-320
44. Proescholdt M.A., Heiss J.D., Walbridge S., Muhlhauser J., Capogrossi M.C., Oldfield E.H., and Merrill M.J. Vascular endothelial growth factor (VEGF) modulates vascular permeability and inflammation in rat brain. J. Neuropathol. Exp. Neurol. 58 (1999) 613-627
45. Ribatti D., Vacca A., Roccaro A.M., Crivellato E., and Presta M. Erythropoietin as an angiogenic factor. Eur. J. Clin. Invest. 33 (2003) 891-896
46. Rosell-Novel A., Montaner J., and Alvarez-Sabin J. Angiogenesis in human cerebral ischemia. Rev. Neurol. 38 (2004) 1076-1082
47. Sawano A., Iwai S., Sakurai Y., Ito M., Shitara K., Nakahata T., and Shibuya M. Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood 97 (2001) 785-791
48. Schoch H.J., Fischer S., and Marti H.H. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125 (2002) 2549-2557
49. Shim J.W., Koh Y.C., Ahn H.K., Park Y.E., Hwang D.Y., and Chi J.G. Expression of bFGF and VEGF in brain astrocytoma. J. Korean Med. Sci. 11 (1996) 149-157
50. Sun Y., Jin K., Xie L., Childs J., Mao X.O., Logvinova A., and Greenberg D.A. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 111 (2003) 1843-1851
51. Tanaka R., Komine-Kobayashi M., Mochizuki H., Yamada M., Furuya T., Migita M., Shimada T., Mizuno Y., and Urabe T. Migration of enhanced green fluorescent protein expressing bone marrow-derived microglia/macrophage into the mouse brain following permanent focal ischemia. Neurosci. 117 (2003) 531-539
52. Tolentino M.J., Miller J.W., Gragoudas E.S., Jakobiec F.A., Flynn E., Chatzistefanou K., Ferrara N., and Adamis A.P. Intravitreous injections of vascular endothelial growth factor produce retinal ischemia and microangiopathy in an adult primate. Ophthalmology 103 (1996) 1820-1828
53. Valable S., Montaner J., Bellail A., Berezowski V., Brillault J., Cecchelli R., Divoux D., Mackenzie E.T., Bernaudin M., Roussel S., and Petit E. VEGF-induced BBB permeability is associated with an MMP-9 activity increase in cerebral ischemia: both effects decreased by Ang-1. J. Cereb. Blood Flow Metab. 25 (2005) 1491-1504
54. van Bruggen N., Thibodeaux H., Palmer J.T., Lee W.P., Fu L., Cairns B., Tumas D., Gerlai R., Williams S.P., van Lookeren Camagne M., and Ferrara N. VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J. Clin. Invest. 104 (1999) 1613-1620
55. Wahlgren N.G., and Ahmed N. Neuroprotection in cerebral ischemia: facts and fancies-the need for new approaches. Cerebrovasc. Dis. 17 (2004) 153-166
56. Waltenberger J., Lange J., and Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: a potential predictor for the individual capacity to develop collaterals. Circulation 102 (2000) 185-190
57. Wang L., Zhang Z., Wang Y., Zhang R., and Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35 (2004) 1732-1737
58. Wang Y., Kilic E., Kilic U., Weber B., Bassetti C.L., Marti H.H., and Hermann D.M. VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 128 (2005) 52-63
59. Wu D. Neuroprotection in experimental stroke with targeted neurotrophins. NeuroRx 2 (2005) 120-128
60. Zhang Z., and Chopp M. Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc. Med. 12 (2002) 62-66
61. Zhang Z.G., Zhang L., Tsang W., Soltanian-Zadeh H., Morris D., Zhang R., Goussev A., Powers C., Yeich T., and Chopp M. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 22 (2002) 379-392