Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Role of Carbon Monoxide in Neurovascular Repair Processing

  • Choi, Yoon Kyung (Department of Integrative Bioscience and Biotechnology, Konkuk University)
  • Received : 2017.07.17
  • Accepted : 2017.08.17
  • Published : 2018.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Carbon monoxide (CO) is a gaseous molecule produced from heme by heme oxygenase (HO). Endogenous CO production occurring at low concentrations is thought to have several useful biological roles. In mammals, especially humans, a proper neurovascular unit comprising endothelial cells, pericytes, astrocytes, microglia, and neurons is essential for the homeostasis and survival of the central nervous system (CNS). In addition, the regeneration of neurovascular systems from neural stem cells and endothelial precursor cells after CNS diseases is responsible for functional repair. This review focused on the possible role of CO/HO in the neurovascular unit in terms of neurogenesis, angiogenesis, and synaptic plasticity, ultimately leading to behavioral changes in CNS diseases. CO/HO may also enhance cellular networks among endothelial cells, pericytes, astrocytes, and neural stem cells. This review highlights the therapeutic effects of CO/HO on CNS diseases involved in neurogenesis, synaptic plasticity, and angiogenesis. Moreover, the cellular mechanisms and interactions by which CO/HO are exploited for disease prevention and their therapeutic applications in traumatic brain injury, Alzheimer's disease, and stroke are also discussed.

Keywords

References

  1. Ahmad, A. S., Zhuang, H. and Dore, S. (2006) Heme oxygenase-1 protects brain from acute excitotoxicity. Neuroscience 141, 1703-1708. https://doi.org/10.1016/j.neuroscience.2006.05.035
  2. Almeida, A. S., Soares, N. L., Vieira, M., Gramsbergen, J. B. and Vieira, H. L. (2016) Carbon Monoxide Releasing Molecule-A1 (CORM-A1) improves neurogenesis: increase of neuronal differentiation yield by preventing cell death. PLoS ONE 11, e0154781. https://doi.org/10.1371/journal.pone.0154781
  3. Araque, A. (2008) Astrocytes process synaptic information. Neuron Glia Biol. 4, 3-10.
  4. Argaw, A. T., Asp, L., Zhang, J., Navrazhina, K., Pham, T., Mariani, J. N., Mahase, S., Dutta, D. J., Seto, J., Kramer, E. G., Ferrara, N., Sofroniew, M. V. and John, G. R. (2012) Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Invest. 122, 2454-2468. https://doi.org/10.1172/JCI60842
  5. Armulik, A., Genove, G., Mae, M., Nisancioglu, M. H., Wallgard, E., Niaudet, C., He, L., Norlin, J., Lindblom, P., Strittmatter, K., Johansson, B. R. and Betsholtz, C. (2010) Pericytes regulate the blood-brain barrier. Nature 468, 557-561. https://doi.org/10.1038/nature09522
  6. Bauer, I. and Pannen, B. H. (2009) Bench-to-bedside review: Carbon monoxide--from mitochondrial poisoning to therapeutic use. Crit. Care 13, 220. https://doi.org/10.1186/cc7887
  7. Bell, R. D., Winkler, E. A., Sagare, A. P., Singh, I., LaRue, B., Deane, R. and Zlokovic, B. V. (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68, 409-427. https://doi.org/10.1016/j.neuron.2010.09.043
  8. Benvenisti-Zarom, L. and Regan, R. F. (2007) Astrocyte-specific heme oxygenase-1 hyperexpression attenuates heme-mediated oxidative injury. Neurobiol. Dis. 26, 688-695. https://doi.org/10.1016/j.nbd.2007.03.006
  9. Bilban, M., Bach, F. H., Otterbein, S. L., Ifedigbo, E., d'Avila, J. C., Esterbauer, H., Chin, B. Y., Usheva, A., Robson, S. C., Wagner, O. and Otterbein, L. E. (2006) Carbon monoxide orchestrates a protective response through $PPAR{\gamma}$. Immunity 24, 601-610. https://doi.org/10.1016/j.immuni.2006.03.012
  10. Canto, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M., Noriega, L., Milne, J. C., Elliott, P. J., Puigserver, P. and Auwerx, J. (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458, 1056-1060. https://doi.org/10.1038/nature07813
  11. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P. and Gurtner, G. C. (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-864.
  12. Chang, E. F., Wong, R. J., Vreman, H. J., Igarashi, T., Galo, E., Sharp, F. R., Stevenson, D. K. and Noble-Haeusslein, L. J. (2003) Heme oxygenase-2 protects against lipid peroxidation-mediated cell loss and impaired motor recovery after traumatic brain injury. J. Neurosci. 23, 3689-3696. https://doi.org/10.1523/JNEUROSCI.23-09-03689.2003
  13. Chen-Roetling, J., Benvenisti-Zarom, L. and Regan, R. F. (2005) Cultured astrocytes from heme oxygenase-1 knockout mice are more vulnerable to heme-mediated oxidative injury. J. Neurosci. Res. 82, 802-810. https://doi.org/10.1002/jnr.20681
  14. Chen-Roetling, J. and Regan, R. F. (2006) Effect of heme oxygenase-1 on the vulnerability of astrocytes and neurons to hemoglobin. Biochem. Biophys. Res. Commun. 350, 233-237. https://doi.org/10.1016/j.bbrc.2006.09.036
  15. Choi, Y. K., Kim, C. K., Lee, H., Jeoung, D., Ha, K. S., Kwon, Y. G., Kim, K. W. and Kim, Y. M. (2010) Carbon monoxide promotes VEGF expression by increasing HIF-$1{\alpha}$ protein level via two distinct mechanisms, translational activation and stabilization of HIF-$1{\alpha}$ protein. J. Biol. Chem. 285, 32116-32125. https://doi.org/10.1074/jbc.M110.131284
  16. Choi, Y. K., Kim, J. H., Lee, D. K., Lee, K. S., Won, M. H., Jeoung, D., Lee, H., Ha, K. S., Kwon, Y. G. and Kim, Y. M. (2017) Carbon monoxide potentiation of L-type $Ca^{2+}$ channel activity increases HIF-$1{\alpha}$-independent VEGF expression via an $AMPK{\alpha}$/SIRT1-mediated PGC-$1{\alpha}/ERR{\alpha}$ axis. Antioxid. Redox Signal. 27, 21-36.
  17. Choi, Y. K., Maki, T., Mandeville, E. T., Koh, S. H., Hayakawa, K., Arai, K., Kim, Y. M., Whalen, M. J., Xing, C., Wang, X., Kim, K. W. and Lo, E. H. (2016a) Dual effects of carbon monoxide on pericytes and neurogenesis in traumatic brain injury. Nat. Med. 22, 1335-1341. https://doi.org/10.1038/nm.4188
  18. Choi, Y. K., Park, J. H., Baek, Y. Y., Won, M. H., Jeoung, D., Lee, H., Ha, K. S., Kwon, Y. G. and Kim, Y. M. (2016b) Carbon monoxide stimulates astrocytic mitochondrial biogenesis via L-type $Ca^{2+}$ channel-mediated PGC-$1{\alpha}/ERR{\alpha}$ activation. Biochem. Biophys. Res. Commun. 479, 297-304.
  19. Chun, Y. J. and Kim, D. (2016) Cancer activation and polymorphisms of human cytochrome P450 1B1. Toxicol. Res. 32, 89-93. https://doi.org/10.5487/TR.2016.32.2.089
  20. Chung, W. S., Welsh, C. A., Barres, B. A. and Stevens, B. (2015) Do glia drive synaptic and cognitive impairment in disease? Nat. Neurosci. 18, 1539-1545. https://doi.org/10.1038/nn.4142
  21. Clark, J. E., Naughton, P., Shurey, S., Green, C. J., Johnson, T. R., Mann, B. E., Foresti, R. and Motterlini, R. (2003) Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ. Res. 93, e2-e8. https://doi.org/10.1161/01.RES.0000084381.86567.08
  22. Dallas, M. L., Yang, Z., Boyle, J. P., Boycott, H. E., Scragg, J. L., Milligan, C. J., Elies, J., Duke, A., Thireau, J., Reboul, C., Richard, S., Bernus, O., Steele, D. S. and Peers, C. (2012) Carbon monoxide induces cardiac arrhythmia via induction of the late $Na^+$ current. Am. J. Respir. Crit. Care Med. 186, 648-656. https://doi.org/10.1164/rccm.201204-0688OC
  23. Daneman, R., Zhou, L., Kebede, A. A. and Barres, B. A. (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468, 562-566. https://doi.org/10.1038/nature09513
  24. Deshane, J., Chen, S., Caballero, S., Grochot-Przeczek, A., Was, H., Li Calzi, S., Lach, R., Hock, T. D., Chen, B., Hill-Kapturczak, N., Siegal, G. P., Dulak, J., Jozkowicz, A., Grant, M. B. and Agarwal, A. (2007) Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J. Exp. Med. 204, 605-618. https://doi.org/10.1084/jem.20061609
  25. Ewing, J. F. and Maines, M. D. (1992) In situ hybridization and immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: differential distribution of isozyme 1 and 2. Mol. Cell. Neurosci. 3, 559-570. https://doi.org/10.1016/1044-7431(92)90068-D
  26. Fayad-Kobeissi, S., Ratovonantenaina, J., Dabire, H., Wilson, J. L., Rodriguez, A. M., Berdeaux, A., Dubois-Rande, J. L., Mann, B. E., Motterlini, R. and Foresti, R. (2016) Vascular and angiogenic activities of CORM-401, an oxidant-sensitive CO-releasing molecule. Biochem. Pharmacol. 102, 64-77. https://doi.org/10.1016/j.bcp.2015.12.014
  27. Fujita, T., Toda, K., Karimova, A., Yan, S. F., Naka, Y., Yet, S. F. and Pinsky, D. J. (2001) Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 7, 598-604. https://doi.org/10.1038/87929
  28. Fukuda, K., Panter, S. S., Sharp, F. R. and Noble, L. J. (1995) Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci. Lett. 199, 127-130. https://doi.org/10.1016/0304-3940(95)12042-3
  29. Garwood, C. J., Ratcliffe, L. E., Simpson, J. E., Heath, P. R., Ince, P. G. and Wharton, S. B. (2017) Review: astrocytes in Alzheimer's disease and other age-associated dementias: a supporting player with a central role. Neuropathol. Appl. Neurobiol. 43, 281-298.
  30. Gursoy-Ozdemir, Y., Can, A. and Dalkara, T. (2004) Reperfusion-induced oxidative/nitrative injury to neurovascular unit after focal cerebral ischemia. Stroke 35, 1449-1453. https://doi.org/10.1161/01.STR.0000126044.83777.f4
  31. Han, S., Pham, T. V., Kim, J. H., Lim, Y. R., Park, H. G., Cha, G. S., Yun, C. H., Chun, Y. J., Kang, L. W. and Kim, D. (2016) Structural analysis of the Streptomyces avermitilis CYP107W1-oligomycin A complex and role of the tryptophan 178 residue. Mol. Cells 39, 211-216. https://doi.org/10.14348/molcells.2016.2226
  32. Hettiarachchi, N., Dallas, M., Al-Owais, M., Griffiths, H., Hooper, N., Scragg, J., Boyle, J. and Peers, C. (2014) Heme oxygenase-1 protects against Alzheimer's amyloid-${\beta}$(1-42)-induced toxicity via carbon monoxide production. Cell Death Dis. 5, e1569. https://doi.org/10.1038/cddis.2014.529
  33. Ikonomovic, M. D., Mi, Z. and Abrahamson, E. E. (2017) Disordered APP metabolism and neurovasculature in trauma and aging: Combined risks for chronic neurodegenerative disorders. Ageing Res. Rev. 34, 51-63. https://doi.org/10.1016/j.arr.2016.11.003
  34. Jeong, Y. H., Park, J. S., Kim, D. H. and Kim, H. S. (2016) Lonchocarpine increases Nrf2/ARE-mediated antioxidant enzyme expression by modulating AMPK and MAPK signaling in brain astrocytes. Biomol. Ther. (Seoul) 24, 581-588. https://doi.org/10.4062/biomolther.2016.141
  35. Jin, C. H., So, Y. K., Han, S. N. and Kim, J. B. (2016) Isoegomaketone upregulates heme oxygenase-1 in RAW264.7 cells via ROS/p38 MAPK/Nrf2 pathway. Biomol. Ther. (Seoul) 24, 510-516. https://doi.org/10.4062/biomolther.2015.194
  36. Kim, J. H., Choi, Y. K., Lee, K. S., Cho, D. H., Baek, Y. Y., Lee, D. K., Ha, K. S., Choe, J., Won, M. H., Jeoung, D., Lee, H., Kwon, Y. G. and Kim, Y. M. (2012) Functional dissection of Nrf2-dependent phase II genes in vascular inflammation and endotoxic injury using Keap1 siRNA. Free Radic. Biol. Med. 53, 629-640 https://doi.org/10.1016/j.freeradbiomed.2012.04.019
  37. Kim, Y. M., Pae, H. O., Park, J. E., Lee, Y. C., Woo, J. M., Kim, N. H., Choi, Y. K., Lee, B. S., Kim, S. R. and Chung, H. T. (2011) Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 14, 137-167. https://doi.org/10.1089/ars.2010.3153
  38. Lancel, S., Hassoun, S. M., Favory, R., Decoster, B., Motterlini, R. and Neviere, R. (2009) Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J. Pharmacol. Exp. Ther. 329, 641-648. https://doi.org/10.1124/jpet.108.148049
  39. Lee, S. W., Kim, W. J., Choi, Y. K., Song, H. S., Son, M. J., Gelman, I. H., Kim, Y. J. and Kim, K. W. (2003) SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat. Med. 9, 900-906. https://doi.org/10.1038/nm889
  40. Li, F. Y., Lam, K. S., Tse, H. F., Chen, C., Wang, Y., Vanhoutte, P. M. and Xu, A. (2012) Endothelium-selective activation of AMP-activated protein kinase prevents diabetes mellitus-induced impairment in vascular function and reendothelialization via induction of heme oxygenase-1 in mice. Circulation 126, 1267-1277. https://doi.org/10.1161/CIRCULATIONAHA.112.108159
  41. Li, N., Lu, X., Zhao, X., Xiang, F. L., Xenocostas, A., Karmazyn, M. and Feng, Q. (2009) Endothelial nitric oxide synthase promotes bone marrow stromal cell migration to the ischemic myocardium via upregulation of stromal cell-derived factor-$1{\alpha}$. Stem Cells 27, 961-970. https://doi.org/10.1002/stem.6
  42. Lin, H. H., Chen, Y. H., Yet, S. F. and Chau, L. Y. (2009) After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J. Thromb. Haemost. 7, 1401-1408. https://doi.org/10.1111/j.1538-7836.2009.03478.x
  43. Lo, E. H., Broderick, J. P. and Moskowitz, M. A. (2004) tPA and proteolysis in the neurovascular unit. Stroke 35, 354-356. https://doi.org/10.1161/01.STR.0000115164.80010.8A
  44. Lynch, D. R. and Dawson, T. M. (1994) Secondary mechanisms in neuronal trauma. Curr. Opin. Neurol. 7, 510-516. https://doi.org/10.1097/00019052-199412000-00007
  45. Maines, M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554. https://doi.org/10.1146/annurev.pharmtox.37.1.517
  46. McCoubrey, W. K., Jr., Huang, T. J. and Maines, M. D. (1997) Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 247, 725-732. https://doi.org/10.1111/j.1432-1033.1997.00725.x
  47. Mintz-Hittner, H. A., Kennedy, K. A. and Chuang, A. Z. (2011) Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. N. Engl. J. Med. 364, 603-615. https://doi.org/10.1056/NEJMoa1007374
  48. Mobarak, C. D., Anderson, K. D., Morin, M., Beckel-Mitchener, A., Rogers, S. L., Furneaux, H., King, P. and Perrone-Bizzozero, N. I. (2000) The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells. Mol. Biol. Cell 11, 3191-3203. https://doi.org/10.1091/mbc.11.9.3191
  49. Motterlini, R., Clark, J. E., Foresti, R., Sarathchandra, P., Mann, B. E. and Green, C. J. (2002) Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ. Res. 90, E17-E24. https://doi.org/10.1161/hh0202.104530
  50. Motterlini, R., Mann, B. E., Johnson, T. R., Clark, J. E., Foresti, R. and Green, C. J. (2003) Bioactivity and pharmacological actions of carbon monoxide-releasing molecules. Curr. Pharm. Des. 9, 2525-2539. https://doi.org/10.2174/1381612033453785
  51. Motterlini, R. and Otterbein, L. E. (2010) The therapeutic potential of carbon monoxide. Nat. Rev. Drug Discov. 9, 728-743. https://doi.org/10.1038/nrd3228
  52. Nada, S. E., Tulsulkar, J. and Shah, Z. A. (2014) Heme oxygenase 1-mediated neurogenesis is enhanced by Ginkgo biloba (EGb 761(R)) after permanent ischemic stroke in mice. Mol. Neurobiol. 49, 945-956. https://doi.org/10.1007/s12035-013-8572-x
  53. Nelson, C. W., Wei, E. P., Povlishock, J. T., Kontos, H. A. and Moskowitz, M. A. (1992) Oxygen radicals in cerebral ischemia. Am. J. Physiol. 263, H1356-H1362.
  54. Pae, H. O., Oh, G. S., Choi, B. M., Kim, Y. M. and Chung, H. T. (2005) A molecular cascade showing nitric oxide-heme oxygenase-1-vascular endothelial growth factor-interleukin-8 sequence in human endothelial cells. Endocrinology 146, 2229-2238. https://doi.org/10.1210/en.2004-1431
  55. Panahian, N., Yoshiura, M. and Maines, M. D. (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187-1203.
  56. Parfenova, H., Basuroy, S., Bhattacharya, S., Tcheranova, D., Qu, Y., Regan, R. F. and Leffler, C. W. (2006) Glutamate induces oxidative stress and apoptosis in cerebral vascular endothelial cells: contributions of HO-1 and HO-2 to cytoprotection. Am. J. Physiol. Cell Physiol. 290, C1399-C1410. https://doi.org/10.1152/ajpcell.00386.2005
  57. Peers, C. (2012) Modulation of ion channels and transporters by carbon monoxide: causes for concern? Front. Physiol. 3, 477.
  58. Poss, K. D., Thomas, M. J., Ebralidze, A. K., O’Dell, T. J. and Tonegawa, S. (1995) Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron 15, 867-873. https://doi.org/10.1016/0896-6273(95)90177-9
  59. Routtenberg, A., Cantallops, I., Zaffuto, S., Serrano, P. and Namgung, U. (2000) Enhanced learning after genetic overexpression of a brain growth protein. Proc. Natl. Acad. Sci. U.S.A. 97, 7657-7662. https://doi.org/10.1073/pnas.97.13.7657
  60. Sagare, A. P., Bell, R. D., Zhao, Z., Ma, Q., Winkler, E. A., Ramanathan, A. and Zlokovic, B. V. (2013) Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat. Commun. 4, 2932. https://doi.org/10.1038/ncomms3932
  61. Scapagnini, G., D'Agata, V., Calabrese, V., Pascale, A., Colombrita, C., Alkon, D. and Cavallaro, S. (2002) Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res. 954, 51-59. https://doi.org/10.1016/S0006-8993(02)03338-3
  62. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732. https://doi.org/10.1038/nrc1187
  63. Shinomura, T., Nakao, S. and Mori, K. (1994) Reduction of depolarization-induced glutamate release by heme oxygenase inhibitor: possible role of carbon monoxide in synaptic transmission. Neurosci. Lett. 166, 131-134. https://doi.org/10.1016/0304-3940(94)90468-5
  64. Snipes, G. J., Chan, S. Y., McGuire, C. B., Costello, B. R., Norden, J. J., Freeman, J. A. and Routtenberg, A. (1987) Evidence for the coidentification of GAP-43, a growth-associated protein, and F1, a plasticity-associated protein. J. Neurosci. 7, 4066-4075. https://doi.org/10.1523/JNEUROSCI.07-12-04066.1987
  65. Spaide, R. F. and Fisher, Y. L. (2006) Intravitreal bevacizumab (Avastin) treatment of proliferative diabetic retinopathy complicated by vitreous hemorrhage. Retina 26, 275-278. https://doi.org/10.1097/00006982-200603000-00004
  66. Stone, J., Itin, A., Alon, T., Pe'er, J., Gnessin, H., Chan-Ling, T. and Keshet, E. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15, 4738-4747. https://doi.org/10.1523/JNEUROSCI.15-07-04738.1995
  67. Suliman, H. B., Carraway, M. S., Tatro, L. G. and Piantadosi, C. A. (2007) A new activating role for CO in cardiac mitochondrial biogenesis. J. Cell Sci. 120, 299-308. https://doi.org/10.1242/jcs.03318
  68. Trakshel, G. M. and Maines, M. D. (1989) Multiplicity of heme oxygenase isozymes. HO-1 and HO-2 are different molecular species in rat and rabbit. J. Biol. Chem. 264, 1323-1328.
  69. Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V. and Snyder, S. H. (1993) Carbon monoxide: a putative neural messenger. Science 259, 381-384. https://doi.org/10.1126/science.7678352
  70. Wang, B., Cao, W., Biswal, S. and Dore, S. (2011) Carbon monoxide-activated Nrf2 pathway leads to protection against permanent focal cerebral ischemia. Stroke 42, 2605-2610. https://doi.org/10.1161/STROKEAHA.110.607101
  71. Wang, J. and Dore, S. (2008) Heme oxygenase 2 deficiency increases brain swelling and inflammation after intracerebral hemorrhage. Neuroscience 155, 1133-1141.
  72. Winkler, E. A., Bell, R. D. and Zlokovic, B. V. (2010) Pericyte-specific expression of PDGF ${\beta}$ receptor in mouse models with normal and deficient PDGF ${\beta}$ receptor signaling. Mol. Neurodegener. 5, 32.
  73. Winkler, E. A., Bell, R. D. and Zlokovic, B. V. (2011) Central nervous system pericytes in health and disease. Nat. Neurosci. 14, 1398-1405.
  74. Winkler, E. A., Sagare, A. P. and Zlokovic, B. V. (2014) The pericyte: a forgotten cell type with important implications for Alzheimer's disease? Brain Pathol. 24, 371-386. https://doi.org/10.1111/bpa.12152
  75. Wu, M. L., Ho, Y. C. and Yet, S. F. (2011) A central role of heme oxygenase-1 in cardiovascular protection. Antioxid. Redox Signal. 15, 1835-1846.
  76. Xing, C. and Lo, E. H. (2017) Help-me signaling: Non-cell autonomous mechanisms of neuroprotection and neurorecovery. Prog. Neurobiol. 152, 181-199. https://doi.org/10.1016/j.pneurobio.2016.04.004
  77. Xiong, Y., Mahmood, A. and Chopp, M. (2013) Animal models of traumatic brain injury. Nat. Rev. Neurosci. 14, 128-142. https://doi.org/10.1038/nrn3407
  78. Yabluchanskiy, A., Sawle, P., Homer-Vanniasinkam, S., Green, C. J., Foresti, R. and Motterlini, R. (2012) CORM-3, a carbon monoxide-releasing molecule, alters the inflammatory response and reduces brain damage in a rat model of hemorrhagic stroke. Crit. Care Med. 40, 544-552. https://doi.org/10.1097/CCM.0b013e31822f0d64
  79. Yemisci, M., Gursoy-Ozdemir, Y., Vural, A., Can, A., Topalkara, K. and Dalkara, T. (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat. Med. 15, 1031-1037.
  80. Zhang, R., Zhang, L., Zhang, Z., Wang, Y., Lu, M., Lapointe, M. and Chopp, M. (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann. Neurol. 50, 602-611. https://doi.org/10.1002/ana.1249
  81. Zhao, Y., Guan, Y. F., Zhou, X. M., Li, G. Q., Li, Z. Y., Zhou, C. C., Wang, P. and Miao, C. Y. (2015) Regenerative neurogenesis after ischemic stroke promoted by nicotinamide phosphoribosyltransferase-nicotinamide adenine dinucleotide cascade. Stroke 46, 1966-1974. https://doi.org/10.1161/STROKEAHA.115.009216
  82. Zhuo, M., Small, S. A., Kandel, E. R. and Hawkins, R. D. (1993) Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260, 1946-1950. https://doi.org/10.1126/science.8100368

Cited by

  1. Carbon Monoxide Ameliorates 6-Hydroxydopamine-Induced Cell Death in C6 Glioma Cells vol.26, pp.2, 2018, https://doi.org/10.4062/biomolther.2018.009
  2. The Heme Oxygenase/Biliverdin Reductase System as Effector of the Neuroprotective Outcomes of Herb-Based Nutritional Supplements vol.10, pp.None, 2018, https://doi.org/10.3389/fphar.2019.01298
  3. The Role of Astrocytes in the Central Nervous System Focused on BK Channel and Heme Oxygenase Metabolites: A Review vol.8, pp.5, 2019, https://doi.org/10.3390/antiox8050121
  4. The Emerging Roles of the Gaseous Signaling Molecules NO, H2S, and CO in the Regulation of Stem Cells vol.6, pp.2, 2020, https://doi.org/10.1021/acsbiomaterials.9b01681
  5. Regenerative Potential of Carbon Monoxide in Adult Neural Circuits of the Central Nervous System vol.21, pp.7, 2018, https://doi.org/10.3390/ijms21072273
  6. Response of the cerebral vasculature to systemic carbon monoxide administration—Regional differences and sexual dimorphism vol.52, pp.1, 2020, https://doi.org/10.1111/ejn.14725
  7. Fine Tuning of Cholinesterase and Glutathione-S-Transferase Activities by Organoruthenium(II) Complexes vol.9, pp.9, 2018, https://doi.org/10.3390/biomedicines9091243
  8. Resistance exercise affects catheter-related thrombosis in rats through miR-92a-3p, oxidative stress and the MAPK/NF-κB pathway vol.21, pp.1, 2018, https://doi.org/10.1186/s12872-021-02233-w