Stem cell factor and granulocyte colony-stimulating factor exhibit therapeutic effects in a mouse model of CADASIL

Neurobiology of Disease

Volumn 73, Issue , 2015, Pages 189-203

  Liu, Xiao Yun ^a   Gonzalez Toledo, Maria E ^a   Fagan, Austin ^b   Duan, Wei Ming ^c,d   Liu, Yanying ^e   Zhang, Siyuan ^a   Li, Bin ^a   Piao, Chun Shu ^a   Nelson, Lila ^a   Zhao, Li Ru ^a,b,c,e  

^a Louisiana State University Health Sciences Center at Shreveport   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

^e State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Angiogenesis; Apoptosis; Bone marrow derived cell; CAA; CADASIL; G CSF; Neurogenesis; SCF; Vascular smooth muscle cell

Indexed keywords

CASPASE 3; GRANULOCYTE COLONY STIMULATING FACTOR; NOTCH3 RECEPTOR; PROTEIN KINASE B; STEM CELL FACTOR; NOTCH RECEPTOR; NOTCH3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CAPILLARY ENDOTHELIAL CELL; CADASIL; CELL DEGENERATION; CELL LOSS; COGNITION; CONTROLLED STUDY; DRUG DOSE INCREASE; IN VITRO STUDY; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NOTCH3 GENE; SMOOTH MUSCLE FIBER; TREATMENT OUTCOME; VASCULAR SMOOTH MUSCLE CELL; ANGIOGENESIS; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; CELL DEATH; COGNITION DISORDERS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; MUTATION; TIME; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE;

ANIMALS; BONE MARROW TRANSPLANTATION; CADASIL; CASPASE 3; CELL DEATH; CELLS, CULTURED; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; GRANULOCYTE COLONY-STIMULATING FACTOR; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGENESIS; RECEPTORS, NOTCH; STEM CELL FACTOR; TIME FACTORS;

EID: 84908691738     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.09.006     Document Type: Article

References (65)

1. Arima K., et al. Cerebral arterial pathology of CADASIL and CARASIL (Maeda syndrome). Neuropathology 2003, 23:327-334.
2. Battisti C., et al. Evaluation of brain apoptosis in a CADASIL postmortem case. Clin. Neuropathol. 2009, 28:358-361.
3. Baudrimont M., et al. Autosomal dominant leukoencephalopathy and subcortical ischemic stroke. A clinicopathological study. Stroke 1993, 24:122-125.
4. Chabriat H., et al. Clinical spectrum of CADASIL: a study of 7 families. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Lancet 1995, 346:934-939.
5. Chabriat H., et al. Cerebral hemodynamics in CADASIL before and after acetazolamide challenge assessed with MRI bolus tracking. Stroke 2000, 31:1904-1912.
6. Choudhary S., et al. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). J. Clin. Aesthet. Dermatol. 2013, 6:29-33.
7. Corti S., et al. Modulated generation of neuronal cells from bone marrow by expansion and mobilization of circulating stem cells with in vivo cytokine treatment. Exp. Neurol. 2002, 177:443-452.
8. Couillard-Despres S., et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 2005, 21:1-14.
9. Culver J.C., et al. A specialized microvascular domain in the mouse neural stem cell niche. PLoS ONE 2013, 8:e53546.
10. Dhandapani K.M., et al. Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappaB. J. Neurochem. 2005, 95:9-19.
11. Dichgans M. Genetics of ischaemic stroke. Lancet Neurol. 2007, 6:149-161.
12. Dichgans M., et al. The phenotypic spectrum of CADASIL: clinical findings in 102 cases. Ann. Neurol. 1998, 44:731-739.
13. Dubroca C., et al. Impaired vascular mechanotransduction in a transgenic mouse model of CADASIL arteriopathy. Stroke 2005, 36:113-117.
14. Fouillade C., et al. Transcriptome analysis for Notch3 target genes identifies Grip2 as a novel regulator of myogenic response in the cerebrovasculature. Arterioscler. Thromb. Vasc. Biol. 2013, 33:76-86.
15. Gahr M., et al. Cerebral amyloidal angiopathy-a disease with implications for neurology and psychiatry. Brain Res. 2013, 1519:19-30.
16. Gomez-Gaviro M.V., et al. Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1317-1322.
17. Ishiko A., et al. Notch3 ectodomain is a major component of granular osmiophilic material (GOM) in CADASIL. Acta Neuropathol. 2006, 112:333-339.
18. Joutel A. Pathogenesis of CADASIL: transgenic and knock-out mice to probe function and dysfunction of the mutated gene, Notch3, in the cerebrovasculature. Bioessays 2011, 33:73-80.
19. Joutel A., et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 1996, 383:707-710.
20. Joutel A., et al. A human homolog of bacterial acetolactate synthase genes maps within the CADASIL critical region. Genomics 1996, 38:192-198.
21. Joutel A., et al. Strong clustering and stereotyped nature of Notch3 mutations in CADASIL patients. Lancet 1997, 350:1511-1515.
22. Joutel A., et al. The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J. Clin. Invest. 2000, 105:597-605.
23. Joutel A., et al. Skin biopsy immunostaining with a Notch3 monoclonal antibody for CADASIL diagnosis. Lancet 2001, 358:2049-2051.
24. Joutel A., et al. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J. Clin. Invest. 2010, 120:433-445.
25. Kalimo H., et al. CADASIL: hereditary disease of arteries causing brain infarcts and dementia. Neuropathol. Appl. Neurobiol. 1999, 25:257-265.
26. Karl C., et al. Neuronal precursor-specific activity of a human doublecortin regulatory sequence. J. Neurochem. 2005, 92:264-282.
27. Kawada H., et al. Administration of hematopoietic cytokines in the subacute phase after cerebral infarction is effective for functional recovery facilitating proliferation of intrinsic neural stem/progenitor cells and transition of bone marrow-derived neuronal cells. Circulation 2006, 113:701-710.
28. Lacar B., et al. S phase entry of neural progenitor cells correlates with increased blood flow in the young subventricular zone. PLoS ONE 2012, 7:e31960.
29. Lacombe P., et al. Impaired cerebral vasoreactivity in a transgenic mouse model of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy arteriopathy. Stroke 2005, 36:1053-1058.
30. Lamagna C., Bergers G. The bone marrow constitutes a reservoir of pericyte progenitors. J. Leukoc. Biol. 2006, 80:677-681.
31. Lesnik Oberstein S.A., et al. Evaluation of diagnostic NOTCH3 immunostaining in CADASIL. Acta Neuropathol. 2003, 106:107-111.
32. Li B., et al. Stem cell factor and granulocyte colony-stimulating factor reduce beta-amyloid deposits in the brains of APP/PS1 transgenic mice. Alzheimers Res. Ther. 2011, 3:8.
33. Mehndiratta P., et al. Cerebral amyloid angiopathy-associated intracerebral hemorrhage: pathology and management. Neurosurg. Focus. 2012, 32:E7.
34. Miao Q., et al. Fibrosis and stenosis of the long penetrating cerebral arteries: the cause of the white matter pathology in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Brain Pathol. 2004, 14:358-364.
35. Miller B., et al. Consequences of reduced cerebral blood flow in brain development. I. Gross morphology, histology, and callosal connectivity. Exp. Neurol. 1993, 124:326-342.
36. Miyamoto N., et al. Crucial role for Ser133-phosphorylated form of cyclic AMP-responsive element binding protein signaling in the differentiation and survival of neural progenitors under chronic cerebral hypoperfusion. Neuroscience 2009, 162:525-536.
37. Monet M., et al. The archetypal R90C CADASIL-NOTCH3 mutation retains NOTCH3 function in vivo. Hum. Mol. Genet. 2007, 16:982-992.
38. Monet-Lepretre M., et al. Distinct phenotypic and functional features of CADASIL mutations in the Notch3 ligand binding domain. Brain 2009, 132:1601-1612.
39. Monet-Lepretre M., et al. Abnormal recruitment of extracellular matrix proteins by excess Notch3 ECD: a new pathomechanism in CADASIL. Brain 2013, 136:1830-1845.
40. Opherk C., et al. Long-term prognosis and causes of death in CADASIL: a retrospective study in 411 patients. Brain 2004, 127:2533-2539.
41. Palsdottir A., et al. Hereditary cystatin C amyloid angiopathy: genetic, clinical, and pathological aspects. Brain Pathol. 2006, 16:55-59.
42. Pescini F., et al. Bone marrow-derived progenitor cells in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Stroke 2010, 41:218-223.
43. Peters N., et al. Spectrum of mutations in biopsy-proven CADASIL: implications for diagnostic strategies. Arch. Neurol. 2005, 62:1091-1094.
44. Piao C.S., et al. The role of stem cell factor and granulocyte-colony stimulating factor in brain repair during chronic stroke. J. Cereb. Blood Flow Metab. 2009, 29:759-770.
45. Plumpe T., et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 2006, 7:77.
46. Ramirez-Castillejo C., et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 2006, 9:331-339.
47. Revesz T., et al. Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol. 2009, 118:115-130.
48. Ruchoux M.M., Maurage C.A. CADASIL: cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. J. Neuropathol. Exp. Neurol. 1997, 56:947-964.
49. Ruchoux M.M., et al. Systemic vascular smooth muscle cell impairment in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Acta Neuropathol. 1995, 89:500-512.
50. Ruchoux M.M., et al. Transgenic mice expressing mutant Notch3 develop vascular alterations characteristic of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Am. J. Pathol. 2003, 162:329-342.
51. Schneider A., et al. The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J. Clin. Invest. 2005, 115:2083-2098.
52. Shen Q., et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004, 304:1338-1340.
53. Shen Q., et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
54. Tavazoie M., et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288.
55. Tikka S., et al. Congruence between NOTCH3 mutations and GOM in 131 CADASIL patients. Brain 2009, 132:933-939.
56. Toth Z.E., et al. The combination of granulocyte colony-stimulating factor and stem cell factor significantly increases the number of bone marrow-derived endothelial cells in brains of mice following cerebral ischemia. Blood 2008, 111:5544-5552.
57. Tuominen S., et al. Positron emission tomography examination of cerebral blood flow and glucose metabolism in young CADASIL patients. Stroke 2004, 35:1063-1067.
58. Villa N., et al. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 2001, 108:161-164.
59. Viswanathan A., et al. Cortical neuronal apoptosis in CADASIL. Stroke 2006, 37:2690-2695.
60. Welte K., et al. Purification and biochemical characterization of human pluripotent hematopoietic colony-stimulating factor. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:1526-1530.
61. Whitman M.C., et al. Blood vessels form a migratory scaffold in the rostral migratory stream. J. Comp. Neurol. 2009, 516:94-104.
62. Zhao L.R., et al. Beneficial effects of hematopoietic growth factor therapy in chronic ischemic stroke in rats. Stroke 2007, 38:2804-2811.
63. Zhao L.R., et al. Brain repair by hematopoietic growth factors in a rat model of stroke. Stroke 2007, 38:2584-2591.
64. Zhu C., et al. Age-dependent regenerative responses in the striatum and cortex after hypoxia-ischemia. J. Cereb. Blood Flow Metab. 2009, 29:342-354.
65. Zsebo K.M., et al. Identification, purification, and biological characterization of hematopoietic stem cell factor from buffalo rat liver-conditioned medium. Cell 1990, 63:195-201.