PDGFR-beta signaling mediates endogenous neurogenesis after postischemic neural stem/progenitor cell transplantation in mice

References

• Barthels D, Das H. Current advances in ischemic stroke research and therapies. Biochim Biophys Acta Mol Basis Dis. 2020;1866(4):165260. doi:10.1016/j.bbadis.2018.09.012.
   PubMed Web of Science ®Google Scholar
• Purvis EM, O’Donnell JC, Chen HI, Cullen DK. Tissue engineering and biomaterial strategies to elicit endogenous neuronal replacement in the brain. Front Neurol. 2020;11:344. doi:10.3389/fneur.2020.00344.
   PubMed Web of Science ®Google Scholar
• Passarelli JP, Nimjee SM, Townsend KL. Stroke and neurogenesis: bridging clinical observations to new mechanistic insights from animal models. Transl Stroke Res. 2022 Dec 3. Epub ahead of print. doi:10.1007/s12975-022-01109-1.
   PubMed Web of Science ®Google Scholar
• de Morree A, Rando TA. Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity. Nat Rev Mol Cell Biol. 2023 Mar 15;24(5):334–54. Epub ahead of print. doi:10.1038/s41580-022-00568-6
   PubMed Web of Science ®Google Scholar
• Urbán N, Cheung TH. Stem cell quiescence: the challenging path to activation. Development. 2021;148(3):dev165084. doi:10.1242/dev.165084.
   PubMed Web of Science ®Google Scholar
• Licht T, Kreisel T, Biala Y, Mohan S, Yaari Y, Anisimov A, Alitalo K, Keshet E. Age-dependent remarkable regenerative potential of the dentate gyrus provided by intrinsic stem cells. J Neurosci. 2020;40(5):974–95. doi:10.1523/JNEUROSCI.1010-19.2019.
   PubMed Web of Science ®Google Scholar
• Kawabori M, Shichinohe H, Kuroda S, Houkin K. Clinical trials of stem cell therapy for cerebral ischemic stroke. Int J Mol Sci. 2020;21(19):7380. doi:10.3390/ijms21197380.
   PubMed Web of Science ®Google Scholar
• Muir KW, Bulters D, Willmot M, Sprigg N, Dixit A, Ward N, Tyrrell P, Majid A, Dunn L, Bath P, et al. Intracerebral implantation of human neural stem cells and motor recovery after stroke: multicentre prospective single-arm study (PISCES-2). J Neurol Neurosurg Psychiatry. 2020;91(4):396–401. doi:10.1136/jnnp-2019-322515.
   PubMed Web of Science ®Google Scholar
• Zhu H, Qiao L, Sun Y, Yin L, Huang L, Jiang L, Li J. Basic fibroblast growth factor enhances cell proliferation in the dentate gyrus of neonatal rats following hypoxic-ischemic brain damage. Neurosci Lett. 2018;673:67–72. doi:10.1016/j.neulet.2018.01.046.
   PubMed Web of Science ®Google Scholar
• Chan SJ, Niu W, Hayakawa K, Hamanaka G, Wang X, Cheah PS, Guo S, Yu Z, Arai K, Selim MH, et al. Promoting neuro-supportive properties of astrocytes with epidermal growth factor hydrogels. Stem Cells Transl Med. 2019;8(12):1242–48. doi:10.1002/sctm.19-0159.
   PubMed Web of Science ®Google Scholar
• Alyautdin R, Ismail NM, Tripathy M, Alyautdin R, Ismail NM. Neuroprotective effect of poly(lactic-co-glycolic acid) nanoparticle-bound brain-derived neurotrophic factor in a permanent middle cerebral artery occlusion model of ischemia in rats. Acta Neurobiol Exp (Wars). 2020;80(1):1–18. doi:10.21307/ane-2020-001.
   PubMed Web of Science ®Google Scholar
• Ge M, Yin J, Qin X, Zhai J, Shao X, Wang R, Fan S, Dai Z, Wang S, Li Y. Isoflurane post-conditioning attenuates cerebral ischemia/reperfusion injury by reducing apoptotic through activating the BMP7/SMAD signaling pathway in rats. J Chem Neuroanat. 2021;112:101916. doi:10.1016/j.jchemneu.2020.101916.
   PubMed Web of Science ®Google Scholar
• Beker M, Caglayan AB, Beker MC, Altunay S, Karacay R, Dalay A, Altintas MO, Kose GT, Hermann DM, Kilic E. Lentivirally administered glial cell line-derived neurotrophic factor promotes post-ischemic neurological recovery, brain remodeling and contralesional pyramidal tract plasticity by regulating axonal growth inhibitors and guidance proteins. Exp Neurol. 2020;331:113364. doi:10.1016/j.expneurol.2020.113364.
   PubMed Web of Science ®Google Scholar
• Shen J, Ishii Y, Xu G, Dang TC, Hamashima T, Matsushima T, Yamamoto S, Hattori Y, Takatsuru Y, Nabekura J, et al. PDGFR-β as a positive regulator of tissue repair in a mouse model of focal cerebral ischemia. J Cereb Blood Flow Metab. 2012;32(2):353–67. doi:10.1038/jcbfm.2011.136.
   PubMed Web of Science ®Google Scholar
• Shen J, Xu G, Zhu R, Yuan J, Ishii Y, Hamashima T, Matsushima T, Yamamoto S, Takatsuru Y, Nabekura J, et al. PDGFR-β restores blood-brain barrier functions in a mouse model of focal cerebral ischemia. J Cereb Blood Flow Metab. 2019;39(8):1501–15. doi:10.1177/0271678X18769515.
   PubMed Web of Science ®Google Scholar
• Ishii Y, Hamashima T, Yamamoto S, Sasahara M. Pathogenetic significance and possibility as a therapeutic target of platelet derived growth factor. Pathol Int. 2017;67(5):235–46. doi:10.1111/pin.12530.
   PubMed Web of Science ®Google Scholar
• Sil S, Periyasamy P, Thangaraj A, Chivero ET, Buch S. PDGF/PDGFR axis in the neural systems. Mol Aspects Med. 2018;62:63–74. doi:10.1016/j.mam.2018.01.006.
   PubMed Web of Science ®Google Scholar
• Xu G, Shen J, Ishii Y, Fukuchi M, Dang TC, Zheng Y, Hamashima T, Fujimori T, Tsuda M, Funa K, et al. Functional analysis of platelet-derived growth factor receptor-beta in neural stem/progenitor cells. Neuroscience. 2013;238:195–208.
   PubMed Web of Science ®Google Scholar
• Bouët V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol. 2007;203(2):555–67. doi:10.1016/j.expneurol.2006.09.006.
   PubMed Web of Science ®Google Scholar
• Yamashita T, Liu W, Matsumura Y, Miyagi R, Zhai Y, Kusaki M, Hishikawa N, Ohta Y, Kim SM, Kwak TH, et al. Novel therapeutic transplantation of induced neural stem cells for stroke. Cell Transplant. 2017;26(3):461–67. doi:10.3727/096368916X692988.
   PubMed Web of Science ®Google Scholar
• Zhang L, Schallert T, Zhang ZG, Jiang Q, Arniego P, Li Q, Lu M, Chopp M. A test for detecting long-term sensorimotor dysfunction in the mouse after focal cerebral ischemia. J Neurosci Methods. 2002;117(2):207–14. doi:10.1016/S0165-0270(02)00114-0.
   PubMed Web of Science ®Google Scholar
• Ueno M, Akiguchi I, Hosokawa M, Kotani H, Kanenishi K, Sakamoto H. Blood-brain barrier permeability in the periventricular areas of the normal mouse brain. Acta Neuropathol. 2000;99(4):385–92. doi:10.1007/s004010051140.
   PubMed Web of Science ®Google Scholar
• Ishii Y, Matsumoto Y, Watanabe R, Elmi M, Fujimori T, Nissen J, Cao Y, Nabeshima Y, Sasahara M, Funa K. Characterization of neuroprogenitor cells expressing the PDGF β-receptor within the subventricular zone of postnatal mice. Mol Cell Neurosci. 2008;37(3):507–18. doi:10.1016/j.mcn.2007.11.006.
   PubMed Web of Science ®Google Scholar
• Sarnat HB. Clinical neuropathology practice guide 5-2013: markers of neuronal maturation. Clin Neuropathol. 2013;32(9):340–69. doi:10.5414/NP300638.
   PubMedGoogle Scholar
• Iihara K, Sasahara M, Hashimoto N, Hazama F. Induction of platelet-derived growth factor β-receptor in focal ischemia of rat brain. J Cereb Blood Flow Metab. 1996;16(5):941–49. doi:10.1097/00004647-199609000-00018.
   PubMed Web of Science ®Google Scholar
• Sakata M, Yanamoto H, Hashimoto N, Iihara K, Tsukahara T, Taniguchi T, Kikuchi H. Induction of infarct tolerance by platelet-derived growth factor against reversible focal ischemia. Brain Res. 1998;784(1–2):250–55. doi:10.1016/S0006-8993(97)01345-0.
   PubMed Web of Science ®Google Scholar
• Tang Z, Arjunan P, Lee C, Li Y, Kumar A, Hou X, Wang B, Wardega P, Zhang F, Dong L, et al. Survival effect of PDGF-CC rescues neurons from apoptosis in both brain and retina by regulating GSK3β phosphorylation. J Exp Med. 2010;207(4):867–80. doi:10.1084/jem.20091704.
   PubMed Web of Science ®Google Scholar
• Renner O, Tsimpas A, Kostin S, Valable S, Petit E, Schaper W, Marti HH. Time- and cell type-specific induction of platelet-derived growth factor receptor-β during cerebral ischemia. Brain Res Mol Brain Res. 2003;113(1–2):44–51. doi:10.1016/S0169-328X(03)00085-8.
   PubMedGoogle Scholar
• Arimura K, Ago T, Kamouchi M, Nakamura K, Ishitsuka K, Kuroda J, Sugimori H, Ooboshi H, Sasaki T, Kitazono T. PDGF receptor β signaling in pericytes following ischemic brain injury. Curr Neurovasc Res. 2012;9(1):1–9. doi:10.2174/156720212799297100.
   PubMed Web of Science ®Google Scholar
• Islam O, Loo TX, Heese K. Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr Neurovasc Res. 2009;6(1):42–53. doi:10.2174/156720209787466028.
   PubMed Web of Science ®Google Scholar
• Mohapel P, Frielingsdorf H, Ha Ggblad J, Zachrisson O, Brundin P. Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience. 2005;132(3):767–76. doi:10.1016/j.neuroscience.2004.11.056.
   PubMed Web of Science ®Google Scholar
• Kwon YK. Expression of brain-derived neurotrophic factor mRNA stimulated by basic fibroblast growth factor and platelet-derived growth factor in rat hippocampal cell line. Mol Cells. 1997;7(3):320–25.
   PubMed Web of Science ®Google Scholar
• Lee SH, Han JH, Choi JH, Huh EY, Kwon YK, Kaang BK. The effect of brain-derived neurotrophic factor on neuritogenesis and synaptic plasticity in aplysia neurons and the hippocampal cell line HiB5. Mol Cells. 2003;15(2):233–39.
   PubMed Web of Science ®Google Scholar
• Sato H, Ishii Y, Yamamoto S, Azuma E, Takahashi Y, Hamashima T, Umezawa A, Mori H, Kuroda S, Endo S, et al. PDGFR-β plays a key role in the ectopic migration of neuroblasts in cerebral stroke. Stem Cells. 2016;34(3):685–98. doi:10.1002/stem.2212.
   PubMed Web of Science ®Google Scholar
• Wang J, Fu X, Zhang D, Yu L, Lu Z, Gao Y, Liu X, Man J, Li S, Li N, et al. Effects of crenolanib, a nonselective inhibitor of PDGFR, in a mouse model of transient middle cerebral artery occlusion. Neuroscience. 2017;364:202–11.
   PubMed Web of Science ®Google Scholar
• Yang Y, Hu X, Qin Q, Kong F, Peng X, Zhao J, Si J, Yang Z, Xie S. Optimal therapeutic conditions for the neural stem cell-based management of ischemic stroke: a systematic review and network meta-analysis based on animal studies. BMC Neurol. 2022;22(1):345. doi:10.1186/s12883-022-02875-z.
   PubMed Web of Science ®Google Scholar
• Lindvall O, Kokaia Z. Stem cells in human neurodegenerative disorders — time for clinical translation? J Clin Invest. 2010;120(1):29–40. doi:10.1172/JCI40543.
   PubMed Web of Science ®Google Scholar
• Lu Y, Jiang L, Li W, Qu M, Song Y, He X, Zhang Z, Yang GY, Wang Y. Optogenetic inhibition of striatal neuronal activity improves the survival of transplanted neural stem cells and neurological outcomes after ischemic stroke in mice. Stem Cells Int. 2017;2017:4364302. doi:10.1155/2017/4364302.
   PubMed Web of Science ®Google Scholar
• Zheng Z, Chopp M, Chen J. Multifaceted roles of pericytes in central nervous system homeostasis and disease. J Cereb Blood Flow Metab. 2020;40:1381–401. doi:10.1177/0271678X20911331.
   PubMed Web of Science ®Google Scholar
• Papadopoulos N, Lennartsson J. The PDGF/PDGFR pathway as a drug target. Mol Aspects Med. 2018;62:75–88. doi:10.1016/j.mam.2017.11.007.
   PubMed Web of Science ®Google Scholar
• Daynac M, Morizur L, Chicheportiche A, Mouthon MA, Boussin FD. Age-related neurogenesis decline in the subventricular zone is associated with specific cell cycle regulation changes in activated neural stem cells. Sci Rep. 2016;6(1):21505. doi:10.1038/srep21505.
   PubMedGoogle Scholar
• Lindvall O, Kokaia Z. Neurogenesis following stroke affecting the adult brain. Cold Spring Harb Perspect Biol. 2015;7(11):a019034. doi:10.1101/cshperspect.a019034.
   PubMed Web of Science ®Google Scholar