Omega-3 polyunsaturated fatty acids enhance cerebral angiogenesis and provide long-term protection after stroke

Neurobiology of Disease

Volumn 68, Issue , 2014, Pages 91-103

  Wang, Jiayin ^a,b   Shi, Yejie ^a,e   Zhang, Lili ^a,e   Zhang, Feng ^a,b,e   Hu, Xiaoming ^a,b,e   Zhang, Wenting ^a   Leak, Rehana K ^a,d,e   Gao, Yanqin ^a,e   Chen, Ling ^a,c   Chen, Jun ^a,b,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

^d DUQUESNE UNIVERSITY   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Angiopoietin 2; Astrocyte; Neuroprotection; Omega 3 polyunsaturated fatty acids; Stroke; VEGF

Indexed keywords

ANGIOPOIETIN 2; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; PHOSPHOLIPASE C GAMMA1; PROTEIN TYROSINE KINASE; VASCULOTROPIN; ACYL COENZYME A DESATURASE; CAENORHABDITIS ELEGANS PROTEIN; FAT-1 PROTEIN, C ELEGANS; GLUCOSE; NEUROPROTECTIVE AGENT;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE CULTURE; BRAIN ISCHEMIA; BRAIN PROTECTION; CELL PROLIFERATION; CEREBRAL REVASCULARIZATION; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANOXIA; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; COCULTURE; COMPLICATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; NERVOUS SYSTEM DISEASES; PATHOLOGY; PHYSIOLOGY; REACTION TIME; STROKE; TIME; TRANSGENIC MOUSE; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; ANOXIA; CAENORHABDITIS ELEGANS PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; FATTY ACID DESATURASES; FATTY ACIDS, OMEGA-3; GLUCOSE; ISCHEMIC ATTACK, TRANSIENT; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; NERVOUS SYSTEM DISEASES; NEUROPROTECTIVE AGENTS; REACTION TIME; STROKE; TIME FACTORS;

EID: 84901034821     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.04.014     Document Type: Article

References (56)

1. Augustin H.G., Koh G.Y., Thurston G., Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 2009, 10:165-177.
2. Bazan N.G. Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol. 2005, 15:159-166.
3. Belayev L., Khoutorova L., Atkins K.D., Bazan N.G. Robust docosahexaenoic acid-mediated neuroprotection in a rat model of transient, focal cerebral ischemia. Stroke 2009, 40:3121-3126.
4. Bozoyan L., Khlghatyan J., Saghatelyan A. Astrocytes control the development of the migration-promoting vasculature scaffold in the postnatal brain via VEGF signaling. J. Neurosci. 2012, 32:1687-1704.
5. Cao G., Minami M., Pei W., Yan C., Chen D., O'Horo C., Graham S.H., Chen J. Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J. Cereb. Blood Flow Metab. 2001, 21:321-333.
6. Connor K.M., SanGiovanni J.P., Lofqvist C., Aderman C.M., Chen J., Higuchi A., Hong S., Pravda E.A., Majchrzak S., Carper D., Hellstrom A., Kang J.X., Chew E.Y., Salem N., Serhan C.N., Smith L.E. Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat. Med. 2007, 13:868-873.
7. Daly C., Eichten A., Castanaro C., Pasnikowski E., Adler A., Lalani A.S., Papadopoulos N., Kyle A.H., Minchinton A.I., Yancopoulos G.D., Thurston G. Angiopoietin-2 functions as a Tie2 agonist in tumor models, where it limits the effects of VEGF inhibition. Cancer Res. 2013, 73:108-118.
8. Dejana E., Orsenigo F., Lampugnani M.G. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 2008, 121:2115-2122.
9. Dimitrijevic O.B., Stamatovic S.M., Keep R.F., Andjelkovic A.V. Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury. J. Cereb. Blood Flow Metab. 2006, 26:797-810.
10. Durham-Lee J.C., Wu Y., Mokkapati V.U., Paulucci-Holthauzen A.A., Nesic O. Induction of angiopoietin-2 after spinal cord injury. Neuroscience 2012, 202:454-464.
11. Eady T.N., Belayev L., Khoutorova L., Atkins K.D., Zhang C., Bazan N.G. Docosahexaenoic acid signaling modulates cell survival in experimental ischemic stroke penumbra and initiates long-term repair in young and aged rats. PLoS One 2012, 7:e46151.
12. Fan Y., Shen F., Frenzel T., Zhu W., Ye J., Liu J., Chen Y., Su H., Young W.L., Yang G.Y. Endothelial progenitor cell transplantation improves long-term stroke outcome in mice. Ann. Neurol. 2010, 67:488-497.
13. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., Lo E.H. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
14. Fox P.L., DiCorleto P.E. Fish oils inhibit endothelial cell production of platelet-derived growth factor-like protein. Science 1988, 241:453-456.
15. Gan Y., Ji X., Hu X., Luo Y., Zhang L., Li P., Liu X., Yan F., Vosler P., Gao Y., Stetler R.A., Chen J. Transgenic overexpression of peroxiredoxin-2 attenuates ischemic neuronal injury via suppression of a redox-sensitive pro-death signaling pathway. Antioxid. Redox Signal. 2012, 17:719-732.
16. Green T.P., Fennell M., Whittaker R., Curwen J., Jacobs V., Allen J., Logie A., Hargreaves J., Hickinson D.M., Wilkinson R.W., Elvin P., Boyer B., Carragher N., Ple P.A., Bermingham A., Holdgate G.A., Ward W.H., Hennequin L.F., Davies B.R., Costello G.F. Preclinical anticancer activity of the potent, oral Src inhibitor AZD0530. Mol. Oncol. 2009, 3:248-261.
17. Hacke W., Kaste M., Bluhmki E., Brozman M., Davalos A., Guidetti D., Larrue V., Lees K.R., Medeghri Z., Machnig T., Schneider D., von K.R., Wahlgren N., Toni D. Thrombolysis with alteplase 3 to 4.5hours after acute ischemic stroke. N. Engl. J. Med. 2008, 359:1317-1329.
18. Holopainen T., Saharinen P., D'Amico G., Lampinen A., Eklund L., Sormunen R., Anisimov A., Zarkada G., Lohela M., Helotera H., Tammela T., Benjamin L.E., Yla-Herttuala S., Leow C.C., Koh G.Y., Alitalo K. Effects of angiopoietin-2-blocking antibody on endothelial cell-cell junctions and lung metastasis. J. Natl. Cancer Inst. 2012, 104:461-475.
19. Hu X., Li P., Guo Y., Wang H., Leak R.K., Chen S., Gao Y., Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012, 43:3063-3070.
20. Hu X., Zhang F., Leak R.K., Zhang W., Iwai M., Stetler R.A., Dai Y., Zhao A., Gao Y., Chen J. Transgenic overproduction of omega-3 polyunsaturated fatty acids provides neuroprotection and enhances endogenous neurogenesis after stroke. Curr. Mol. Med. 2013, 13:1465-1473.
21. Ishikawa H., Tajiri N., Shinozuka K., Vasconcellos J., Kaneko Y., Lee H.J., Mimura O., Dezawa M., Kim S.U., Borlongan C.V. Vasculogenesis in experimental stroke after human cerebral endothelial cell transplantation. Stroke 2013, 44:3473-3481.
22. Jones N., Iljin K., Dumont D.J., Alitalo K. Tie receptors: new modulators of angiogenic and lymphangiogenic responses. Nat. Rev. Mol. Cell Biol. 2001, 2:257-267.
23. Kang J.X., Wang J., Wu L., Kang Z.B. Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature 2004, 427:504.
24. Kim I., Kim H.G., Moon S.O., Chae S.W., So J.N., Koh K.N., Ahn B.C., Koh G.Y. Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ. Res. 2000, 86:952-959.
25. Kim H.J., Vosseler C.A., Weber P.C., Erl W. Docosahexaenoic acid induces apoptosis in proliferating human endothelial cells. J. Cell. Physiol. 2005, 204:881-888.
26. Krupinski J., Kaluza J., Kumar P., Kumar S., Wang J.M. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994, 25:1794-1798.
27. Lee B., Clarke D., Al A.A., Kahle M., Parham C., Auckland L., Shaw C., Fidanboylu M., Orr A.W., Ogunshola O., Fertala A., Thomas S.A., Bix G.J. Perlecan domain V is neuroprotective and proangiogenic following ischemic stroke in rodents. J. Clin. Invest. 2011, 121:3005-3023.
28. Liang S., Pong K., Gonzales C., Chen Y., Ling H.P., Mark R.J., Boschelli F., Boschelli D.H., Ye F., Barrios Sosa A.C., Mansour T.S., Frost P., Wood A., Pangalos M.N., Zaleska M.M. Neuroprotective profile of novel SRC kinase inhibitors in rodent models of cerebral ischemia. J. Pharmacol. Exp. Ther. 2009, 331:827-835.
29. Liu J., Wang Y., Akamatsu Y., Lee C.C., Stetler R.A., Lawton M.T., Yang G.Y. Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog. Neurobiol. 2014, 115C:138-156.
30. Lobov I.B., Brooks P.C., Lang R.A. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11205-11210.
31. Maisonpierre P.C., Suri C., Jones P.F., Bartunkova S., Wiegand S.J., Radziejewski C., Compton D., McClain J., Aldrich T.H., Papadopoulos N., Daly T.J., Davis S., Sato T.N., Yancopoulos G.D. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997, 277:55-60.
32. Mukutmoni-Norris M., Hubbard N.E., Erickson K.L. Modulation of murine mammary tumor vasculature by dietary n-3 fatty acids in fish oil. Cancer Lett. 2000, 150:101-109.
33. Musiek E.S., Brooks J.D., Joo M., Brunoldi E., Porta A., Zanoni G., Vidari G., Blackwell T.S., Montine T.J., Milne G.L., McLaughlin B., Morrow J.D. Electrophilic cyclopentenone neuroprostanes are anti-inflammatory mediators formed from the peroxidation of the omega-3 polyunsaturated fatty acid docosahexaenoic acid. J. Biol. Chem. 2008, 283:19927-19935.
34. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425:479-494.
35. Park J.A., Lee H.S., Ko K.J., Park S.Y., Kim J.H., Choe G., Kweon H.S., Song H.S., Ahn J.C., Yu Y.S., Kim K.W. Meteorin regulates angiogenesis at the gliovascular interface. Glia 2008, 56:247-258.
36. Petty M.A., Lo E.H. Junctional complexes of the blood-brain barrier: permeability changes in neuroinflammation. Prog. Neurobiol. 2002, 68:311-323.
37. Rose D.P., Connolly J.M. Antiangiogenicity of docosahexaenoic acid and its role in the suppression of breast cancer cell growth in nude mice. Int. J. Oncol. 1999, 15:1011-1015.
38. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 2000, 182:311-322.
39. Spencer L., Mann C., Metcalfe M., Webb M., Pollard C., Spencer D., Berry D., Steward W., Dennison A. The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential. Eur. J. Cancer 2009, 45:2077-2086.
40. Stetler R.A., Cao G., Gao Y., Zhang F., Wang S., Weng Z., Vosler P., Zhang L., Signore A., Graham S.H., Chen J. Hsp27 protects against ischemic brain injury via attenuation of a novel stress-response cascade upstream of mitochondrial cell death signaling. J. Neurosci. 2008, 28:13038-13055.
41. Su H., Takagawa J., Huang Y., Arakawa-Hoyt J., Pons J., Grossman W., Kan Y.W. Additive effect of AAV-mediated angiopoietin-1 and VEGF expression on the therapy of infarcted heart. Int. J. Cardiol. 2009, 133:191-197.
42. Summy J.M., Trevino J.G., Lesslie D.P., Baker C.H., Shakespeare W.C., Wang Y., Sundaramoorthi R., Metcalf C.A., Keats J.A., Sawyer T.K., Gallick G.E. AP23846, a novel and highly potent Src family kinase inhibitor, reduces vascular endothelial growth factor and interleukin-8 expression in human solid tumor cell lines and abrogates downstream angiogenic processes. Mol. Cancer Ther. 2005, 4:1900-1911.
43. Szymczak M., Murray M., Petrovic N. Modulation of angiogenesis by omega-3 polyunsaturated fatty acids is mediated by cyclooxygenases. Blood 2008, 111:3514-3521.
44. Towfighi A., Saver J.L. Stroke declines from third to fourth leading cause of death in the United States: historical perspective and challenges ahead. Stroke 2011, 42:2351-2355.
45. Tsuzuki T., Shibata A., Kawakami Y., Nakagawa K., Miyazawa T. Conjugated eicosapentaenoic acid inhibits vascular endothelial growth factor-induced angiogenesis by suppressing the migration of human umbilical vein endothelial cells. J. Nutr. 2007, 137:641-646.
46. Turgeon J., Dussault S., Maingrette F., Groleau J., Haddad P., Perez G., Rivard A. Fish oil-enriched diet protects against ischemia by improving angiogenesis, endothelial progenitor cell function and postnatal neovascularization. Atherosclerosis 2013, 229:295-303.
47. Wei D., Li J., Shen M., Jia W., Chen N., Chen T., Su D., Tian H., Zheng S., Dai Y., Zhao A. Cellular production of n-3 PUFAs and reduction of n-6-to-n-3 ratios in the pancreatic beta-cells and islets enhance insulin secretion and confer protection against cytokine-induced cell death. Diabetes 2010, 59:471-478.
48. Yang S.P., Morita I., Murota S.I. Eicosapentaenoic acid attenuates vascular endothelial growth factor-induced proliferation via inhibiting Flk-1 receptor expression in bovine carotid artery endothelial cells. J. Cell. Physiol. 1998, 176:342-349.
49. Yin K.J., Hamblin M., Chen Y.E. Angiogenesis-regulating microRNAs and ischemic stroke. Curr. Vasc. Pharmacol. 2013, (Epub ahead of print).
50. Zachary I. Signaling mechanisms mediating vascular protective actions of vascular endothelial growth factor. Am. J. Physiol. Cell Physiol. 2001, 280:C1375-C1386.
51. Zan L., Zhang X., Xi Y., Wu H., Song Y., Teng G., Li H., Qi J., Wang J. Src regulates angiogenic factors and vascular permeability after focal cerebral ischemia-reperfusion. Neuroscience 2014, 262:118-128.
52. Zhang Z.G., Chopp M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol. 2009, 8:491-500.
53. Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., Bruggen N., Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 2000, 106:829-838.
54. Zhang W., Hu X., Yang W., Gao Y., Chen J. Omega-3 polyunsaturated fatty acid supplementation confers long-term neuroprotection against neonatal hypoxic-ischemic brain injury through anti-inflammatory actions. Stroke 2010, 41:2341-2347.
55. Zhang M., Wang S., Mao L., Leak R.K., Shi Y., Zhang W., Hu X., Sun B., Cao G., Gao Y., Xu Y., Chen J., Zhang F. Omega-3 fatty acids protect the brain against ischemic injury by activating Nrf2 and upregulating heme oxygenase 1. J. Neurosci. 2014, 34:1903-1915.
56. Zhu Y., Lee C., Shen F., Du R., Young W.L., Yang G.Y. Angiopoietin-2 facilitates vascular endothelial growth factor-induced angiogenesis in the mature mouse brain. Stroke 2005, 36:1533-1537.