Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium
It is challenging to revitalize ischemic penumbra after an acute stroke with intracranial perfusion insufficiency. To evaluate whether cranial burr hole and erythropoietin (EPO) generate effective revascularization, we investigated the efficacy of the augmentation method for reverse arteriogenesis f...
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| Format: | Article |
| Language: | English |
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Elsevier
2019-12-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996119302062 |
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| author | Geun Hwa Park Hee Sun Shin Eun Sil Choi Bok Seon Yoon Mun Hee Choi Seong-Joon Lee Kyung-Eon Lee Jin Soo Lee Ji Man Hong |
| author_facet | Geun Hwa Park Hee Sun Shin Eun Sil Choi Bok Seon Yoon Mun Hee Choi Seong-Joon Lee Kyung-Eon Lee Jin Soo Lee Ji Man Hong |
| author_sort | Geun Hwa Park |
| collection | DOAJ |
| description | It is challenging to revitalize ischemic penumbra after an acute stroke with intracranial perfusion insufficiency. To evaluate whether cranial burr hole and erythropoietin (EPO) generate effective revascularization, we investigated the efficacy of the augmentation method for reverse arteriogenesis from the healthy extracranial milieu. An intracranial perfusion insufficiency was created through bilateral internal carotid artery ligation (bICAL) in Sprague-Dawley rats. We administered recombinant human EPO (5000 U/kg) or saline intraperitoneally for 3 days after bICAL. Mechanical barrier disruption (MBD) was performed through a cranial burr hole with small dural cracks in the right hemisphere. The ipsilateral hemisphere with MBD grossly showed vascular networks between the extra- and intra-cranial spaces 2 weeks after the MBD procedure. It also showed significantly increased vessels in the intracranial vasculature adjacent to the MBD region (p = 0.0006). The levels of pro-angiogenic and inflammatory factors with prominent markers of vessel permeability were also significantly increased (MBD-only vs. control; Tnf-α, p = 0.0007; Vegf, p = 0.0206). In the EPO-administered group, such elevations in inflammation were significantly mitigated (combined vs. MBD-only; Tnf-α, p = 0.0008). The ipsilateral hemisphere with MBD-EPO (vs. MBD-only) showed significantly increased vessels (RECA-1, p = 0.0182) and their maturation (RECA-1/α-SMA, p = 0.0046), with upregulation of tumor growth factor-β1 (Tgf-β1, p = 0.037) and matrix metalloproteinase-2 (Mmp-2, p = 0.0488). These findings were completely blocked by minocycline (MIC) administration during in vivo (Tgf-β1, p = 0.0009; Mmp-2, p < 0.0001) and in vitro experiments (tube formation, p < 0.0001). Our data suggest that the MBD procedure (for angiogenic routes) and EPO administration (for an arteriogenic booster) are complimentary and can facilitate successfully “reverse arteriogenesis” in subjects with intracranial perfusion insufficiency. |
| first_indexed | 2024-12-16T06:09:45Z |
| format | Article |
| id | doaj.art-21279341ce7f4d4da35dc7c1c90e76e1 |
| institution | Directory Open Access Journal |
| issn | 1095-953X |
| language | English |
| last_indexed | 2024-12-16T06:09:45Z |
| publishDate | 2019-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj.art-21279341ce7f4d4da35dc7c1c90e76e12022-12-21T22:41:25ZengElsevierNeurobiology of Disease1095-953X2019-12-01132Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracraniumGeun Hwa Park0Hee Sun Shin1Eun Sil Choi2Bok Seon Yoon3Mun Hee Choi4Seong-Joon Lee5Kyung-Eon Lee6Jin Soo Lee7Ji Man Hong8Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, South KoreaDepartment of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, South KoreaDepartment of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, South KoreaDepartment of Neurology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South KoreaDepartment of Neurology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South KoreaDepartment of Neurology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South KoreaDepartment of Life and Nanopharmaceutical Sciences, Kyung Hee University School of Pharmacy, Seoul, South KoreaDepartment of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, South Korea; Department of Neurology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South KoreaDepartment of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, South Korea; Department of Neurology, Ajou University School of Medicine, Ajou University Medical Center, Suwon, South Korea; Corresponding author at: Department of Neurology, School of Medicine, Ajou University, 164, World cup-ro, Yeongtong-gu, Suwon-si, Gyeonggi-do 16499, South Korea.It is challenging to revitalize ischemic penumbra after an acute stroke with intracranial perfusion insufficiency. To evaluate whether cranial burr hole and erythropoietin (EPO) generate effective revascularization, we investigated the efficacy of the augmentation method for reverse arteriogenesis from the healthy extracranial milieu. An intracranial perfusion insufficiency was created through bilateral internal carotid artery ligation (bICAL) in Sprague-Dawley rats. We administered recombinant human EPO (5000 U/kg) or saline intraperitoneally for 3 days after bICAL. Mechanical barrier disruption (MBD) was performed through a cranial burr hole with small dural cracks in the right hemisphere. The ipsilateral hemisphere with MBD grossly showed vascular networks between the extra- and intra-cranial spaces 2 weeks after the MBD procedure. It also showed significantly increased vessels in the intracranial vasculature adjacent to the MBD region (p = 0.0006). The levels of pro-angiogenic and inflammatory factors with prominent markers of vessel permeability were also significantly increased (MBD-only vs. control; Tnf-α, p = 0.0007; Vegf, p = 0.0206). In the EPO-administered group, such elevations in inflammation were significantly mitigated (combined vs. MBD-only; Tnf-α, p = 0.0008). The ipsilateral hemisphere with MBD-EPO (vs. MBD-only) showed significantly increased vessels (RECA-1, p = 0.0182) and their maturation (RECA-1/α-SMA, p = 0.0046), with upregulation of tumor growth factor-β1 (Tgf-β1, p = 0.037) and matrix metalloproteinase-2 (Mmp-2, p = 0.0488). These findings were completely blocked by minocycline (MIC) administration during in vivo (Tgf-β1, p = 0.0009; Mmp-2, p < 0.0001) and in vitro experiments (tube formation, p < 0.0001). Our data suggest that the MBD procedure (for angiogenic routes) and EPO administration (for an arteriogenic booster) are complimentary and can facilitate successfully “reverse arteriogenesis” in subjects with intracranial perfusion insufficiency.http://www.sciencedirect.com/science/article/pii/S0969996119302062AngiogenesisArteriogenesisErythropoietinIschemic strokeCranial burr hole |
| spellingShingle | Geun Hwa Park Hee Sun Shin Eun Sil Choi Bok Seon Yoon Mun Hee Choi Seong-Joon Lee Kyung-Eon Lee Jin Soo Lee Ji Man Hong Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium Neurobiology of Disease Angiogenesis Arteriogenesis Erythropoietin Ischemic stroke Cranial burr hole |
| title | Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| title_full | Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| title_fullStr | Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| title_full_unstemmed | Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| title_short | Cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| title_sort | cranial burr hole with erythropoietin administration induces reverse arteriogenesis from the enriched extracranium |
| topic | Angiogenesis Arteriogenesis Erythropoietin Ischemic stroke Cranial burr hole |
| url | http://www.sciencedirect.com/science/article/pii/S0969996119302062 |
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