Restoration of cerebral and systemic microvascular architecture in APP/PS1 transgenic mice following treatment with liraglutide™

Microcirculation

Volumn 22, Issue 2, 2015, Pages 133-145

  Kelly, Patricia ^a   Mcclean, Paula L ^a   Ackermann, Maximilian ^b   Konerding, Moritz A ^b   Hölscher, Christian ^c   Mitchell, Christopher A ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; APP PS1 mice; Glucagon like peptide 1; Liraglutide; Microvascular corrosion casting; Scanning electron microscopy

Indexed keywords

AMYLOID BETA PROTEIN; LIRAGLUTIDE; AMYLOID PRECURSOR PROTEIN; ANTIDIABETIC AGENT; GLUCAGON LIKE PEPTIDE 1; PRESENILIN 1; PRESENILIN 1, MOUSE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ARTERY ANEURYSM; BRAIN BLOOD VESSEL; CONTROLLED STUDY; EXTRAVASATION; FEMALE; GLOMERULUS; INCIDENCE; KIDNEY BLOOD VESSEL; MALE; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCANNING ELECTRON MICROSCOPY; SINUS VENOSUS; SPLEEN; TRANSGENIC MOUSE; ULTRASTRUCTURE; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; BRAIN CIRCULATION; DRUG EFFECTS; GENETICS; HUMAN; KIDNEY; METABOLISM; MICROCIRCULATION; PATHOLOGY; PATHOPHYSIOLOGY; VASCULARIZATION;

MUS; MUS MUSCULUS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CEREBROVASCULAR CIRCULATION; GLUCAGON-LIKE PEPTIDE 1; HUMANS; HYPOGLYCEMIC AGENTS; KIDNEY; MICE; MICE, TRANSGENIC; MICROCIRCULATION; MICROVESSELS; PRESENILIN-1; SPLEEN;

EID: 84922681924     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12186     Document Type: Article

References (78)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25, 2010.
2. Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53, 2006.
3. Ackermann M, Houdek JP, Gibney BC, Ysasi A, Wagner W, Belle J, Schittny JC, Enzmann F, Tsuda A, Mentzer SJ, Konerding MA. Sprouting and intussusceptive angiogenesis in postneumonectomy lung growth: mechanisms of alveolar neovascularisation. Angiogenesis 17: 541-551, 2014.
4. Aharinejad SH, Lametshwandtner A. Microvascular Corrosion Casting in Scanning Electron Microscopy: Techniques and Applications. Vienna: Springer, 1992.
5. Arkill KP, Qvortrup K, Starborg T, Mantell JM, Knupp C, Michel CC, Harper SJ, Salmon AH, Squire JM, Bates DO, Neal CR. Resolution of the three dimensional structure of components of the glomerular filtration barrier. BMC Nephrol 1: 15-24, 2014.
6. Beckmann N, Schuler A, Mueggler T, Meyer EP, Wiederhold KH, Staufenbiel M, Krucker T. Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease. J Neurosci 17: 8453-8459, 2003.
7. Benedict C, Hallschmid M, Hatke A, Schultes B, Fehm HL, Born J, Kern W. Intranasal insulin improves memory in humans. Psychoneuroendocrinology 29: 1326-1334, 2004.
8. Bouras C, Kövari E, Herrmann F, Rivara CB, Bailey TL, von Gunten A, Hof PR, Giannakopoulos P. Stereologic analysis of microvascular morphology in the elderly: Alzheimer disease pathology and cognitive status. J Neuropathol Exp Neurol 65: 235-244, 2006.
9. Caduff JH, Fischer LC, Burri PH. Scanning electron microscope study of the developing microvasculature in the postnatal rat lung. Anat Rec 216: 154-164, 1986.
10. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M. Statins induce angiogenesis, neurogenesis and synaptogenesis after stroke. Ann Neurol 53: 743-751, 2003.
11. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276: 21562-21570, 2001.
12. Coyne EF, Ngai AC, Meno JR, Winn HR. Methods for isolation and characterisation of intraerebral arterioles in the C57/BL6 wild-type mouse. J Neurosci Methods 120: 145-153, 2002.
13. Craft S. The role of metabolic disorders in Alzheimer's disease and vascular dementia: two roads converged. Arch Neurol 66: 300-305, 2009.
14. De la Monte SM, Wands JR. Review of insulin and insulin-like growth factor expression, signaling and malfunction in the central nervous system: relevance to Alzheimer's disease. J Alzheimers Dis 7: 45-61, 2005.
15. Deen WM, Lazzara MJ, Myers BD. Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 281: 579-596, 2001.
16. Dill MT, Rothweiler S, Djonov V, Hlushchuck R, Tornillo L, Terracciano L, Meili-Butz S, Radtke F, Heim MH, Semela D. Disruption of Notch 1 induces vascular remodeling, intussusceptive angiogenesis, and angiosarcomas in livers of mice. Gastroenterology 142: 967-977, 2012.
17. Djonov V, Schmid M, Tschanz SA, Burri PH. Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res 86: 286-292, 2000.
18. Dorr A, Sahota B, Chinta LV, Brown ME, Lai AY, Ma K, Hawkes CA, McLaurin J, Stefanovic B. Amyloid-β-dependent compromise of microvascular structure and function in a model of Alzheimer's disease. Brain 135: 3039-3050, 2012.
19. During MJ, Cao L, Zuzga DS, Francis JS, Fitzsimons HL, Jiao X, Bland RJ, Klugmann M, Banks WA, Drucker DJ, Haile CN. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 9: 1173-1179, 2003.
20. Fischer VW, Siddiqi A, Yusufaly Y. Altered angioarchitecture in selected areas of brains with Alzheimer's disease. Acta Neuropathol 79: 672-679, 1990.
21. Freiherr J, Hallschmid M, Frey WH, Brunner YF, Chapman CD, Hölscher C, Craft S, DeFelice FG, Benedict C. Intranasal insulin as a treatment for Alzheimer's disease: a review of basic research and clinical evidence. CNS Drugs 27: 505-514, 2013.
22. Fujita H, Morii T, Fujishma H, Soto T, Shimizu T, Hosoba M, Tsukiyama K, Narita T, Takahashi T, Drucker DJ, Seino Y, Yamada Y. The protective roles of GLP-1R signalling in diabetic nephropathy: possible mechanism and therapeutic potential. Kidney Int 85: 579-589, 2014.
23. swe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24: 516-524, 2006.
24. -/- mouse model. Diab Vasc Dis Res 8: 117-124, 2011.
25. -/- mouse model. Diab Vasc Dis Res 10: 353-360, 2013.
26. Gianni-Barrera R, Trani M, Fontanellaz C, Heberer M, Djonov V, Hlushchuk R, Banfi A. VEGF over-expression in skeletal muscle induces angiogenesis by intussusception rather than sprouting. Angiogenesis 16: 123-136, 2013.
27. Hamilton A, Hölscher C. Receptors for the incretin glucagon-like peptide-1 are expressed on neurons in the central nervous system. NeuroReport 20: 1161-1166, 2009.
28. Hölscher C. Diabetes as a risk factor for Alzheimer's disease: insulin signalling impairment in the brain as an alternative model of Alzheimer's disease. Biochem Soc Trans 39: 891-897, 2011.
29. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR. Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: evidence for augmentation of a 42-specific γ secretase. Hum Mol Genet 13: 159-170, 2004.
30. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17: 157-165, 2001.
31. Kandimalla KK, Curran GL, Holasek SS, Gilles EJ, Wengenack TM, Poduslo JF. Pharmacokinetic analysis of the blood-brain barrier transport of 125I-Amyloid-β protein 40 in wild-type and Alzheimer's disease transgenic mice (APP, PS1) and its implications for amyloid plaque formation. J Pharmacol Exp Ther 313: 1370-1378, 2005.
32. Kastin AJ, Akerstrom V, Pan W. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 18: 7-14, 2002.
33. Kieffer TJ, McIntosh CH, Pederson RA. Degradation of glucose-dependent insulinotropic polypeptide and truncated glucagon-like peptide-1 in vitro and in vivo by dipeptidyl peptidase IV. Endocrinology 136: 3585-3596, 1995.
34. Kitaguchi H, Ihara M, Saiki H, Takahashi R, Tomimoto H. Capillary beds are decreased in Alzheimer's disease, but not in Binswanger's disease. Neurosci Lett 417: 128-131, 2007.
35. Knopman DS. Invited commentary - albuminuria and microvascular disease of the brain - a shared pathophysiology. Am J Epidemiol 171: 287-289, 2010.
36. Konerding MA, Gibney BC, Houdek JP, Chamoto K, Ackermann M, Lee GS, Lin M, Tsuda A, Mentzer SJ. Spatial dependence of alveolar angiogensis in post-pneumonectomy lung growth. Angiogenesis 15: 23-32, 2012.
37. Konerding MA, Turhan A, Ravnic DJ, Lin M, Fuchs C, Secomb TW, Tsuda A, Mentzer SJ. Inflammation-induced intussusceptive angiogenesis in murine colitis. Anat Rec 293: 849-857, 2010.
38. Krucker T, Schuler A, Meyer EP, Staufenbiel M, Beckmann N. Magnetic resonance angiography and vascular corrosion casting as tools in biomedical research: application to transgenic mice modeling Alzheimer's disease. Neurol Res 26: 507-516, 2004.
39. Lametschwandtner A, Lametschwandtner U, Weiger T. Scanning electron microscopy of vascular corrosion casts - techniques and applications: updated review. Scanning Microsc 4: 889-940, 1990.
40. Liu H, Dear AE, Knudsen LB, Simpson RW. A long-acting glucagon-like peptide-1 analogue attenuates induction of plasminogen activator inhibitor type-1 and vascular adhesion molecules. J Endocrinol 201: 59-66, 2009.
41. Lu D, Goussev A, Chen J, Pannu P, Li Y, Mahmood A, Chopp M. Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J Neurotrauma 21: 21-32, 2004.
42. Mackic JB, Weiss MH, Miao W, Kirkmann E, Ghiso J, Calero M, Bading J, Frangione B, Zlokovic BV. Cerebrovascular accumulation and increased blood-brain barrier permeability to circulating Alzheimer's amyloid β peptide in aged squirrel monkey with cerebral amyloid angiopathy. J Neurochem 70: 210-215, 1998.
43. Makanya AN, Hlushchuk R, Djonov VG. Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning and remodeling. Angiogenesis 12: 113-123, 2009.
44. Malm-Erjefalt M, Bjornsdottir I, Vanggaard J, Helleberg H, Larsen U, Oosterhuis B, van Lier JJ, Zdravkovic M, Olsen AK. Metabolism and excretion of the once-daily human glucagon-like peptide-1 analog Liraglutide in healthy male subjects and its in vitro degradation by dipeptidyl peptidase IV and neutral endopeptidase. Drug Metab Dispos 38: 1944-1953, 2010.
45. Mandybur TI. The incidence of cerebral amyloid angiopathy in Alzheimer's disease. Neurology 25: 120-126, 1975.
46. Marques MA, Kulstad JJ, Savard CE, Green PS, Lee SP, Craft S, Watson GS, Cook DG. Peripheral amyloid-β levels regulate amyloid-β clearance from the central nervous system. J Alzheimers Dis 16: 325-329, 2009.
47. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC, Yarasheski KE, Bateman RJ. Decreased clearance of CNS β-amyloid in Alzheimer's disease. Science 330: 1774, 2010.
48. McClean PL, Parthsarathy V, Faivre E, Hölscher C. The diabetes drug Liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci 31: 6587-6594, 2011.
49. Mentzer SJ, Konerding MA. Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 17: 499-509, 2014.
50. Meyer EP, Ulmann-Schuler A, Staufenbiel M, Krucker T. Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer's disease. PNAS 105: 3587-3592, 2008.
51. Minogue AM, Jones RS, Kelly RJ, McDonald CL, Connor TJ, Lynch MA. Age-associated dysregulation of microglial activation is coupled with enhanced blood-brain barrier permeability and pathology in APP/PS1 mice. Neurobiol Aging 35: 1442-1452, 2014.
52. Murakami T. Application of the scanning electron microscope to the study of the fine distribution of blood vessels. Arch Histol Jpn 32: 445-454, 1971.
53. Nauck MA, Holst JJ, Willms B, Schmiegel W. Glucagon-like peptide 1 (GLP-1) as a new therapeutic approach for type-2 diabetes. Exp Clin Endocrinol Diabetes 105: 187-195, 1997.
54. Nisimura LM, Estato V, de Souza EM, Reis PA, Lessa MA, Castro-Faria-Neto HC, de Souza Pereira MC, Tibirica E, Garzoni LR. Acute Chagas disease induces cerebral microvasculopathy in mice. PLoS Negl Trop Dis 8: e2998, 2014.
55. Nyström T, Gutniak MK, Zhang Q, Zhang F, Holst JJ, Ahren B, Sjöholm A. Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am J Physiol Endocrinol Metab 287: 1209-1215, 2004.
56. Okerson T, Chilton RJ. The cardiovascular effects of GLP-1 receptor agonists. Cardiovasc Ther 30: 146-155, 2012.
57. Patan S, Munn LL, Jain RK. Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft; a novel mechanism of tumor angiogenesis. Microvasc Res 51: 260-272, 1996.
58. Perry TA, Greig NH. The glucagon-like peptides: a new genre in therapeutic targets for intervention in Alzheimer's disease. J Alzheimers Dis 4: 487-496, 2002.
59. Rasband WS. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/, 1997-2012.
60. Reger MA, Watson GS, Green PS, Wilkinson CW, Baker LD, Cholerton B, Fishel MA, Plymate SR, Breitner JCS, DeGroodt W, Mehta P, Craft S. Intranasal insulin improves cognition and modulates β-amyloid in early AD. Neurology 70: 440-448, 2008.
61. Rogers AB, Dintzis RZ. Liver and gallbladder. In: Comparative Anatomy and Histology a Mouse and Human Atlas, edited by Treuting PM, Dintzis SM. London: Elsevier, 2012, p. 193-201.
62. Salmon AH, Satchell SC. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. J Pathol 226: 562-574, 2012.
63. Schiöth HB, Craft S, Brooks SJ, Frey WH, Benedict C. Brain insulin signaling and Alzheimer's disease: current evidence and future directions. Mol Neurobiol 46: 4-10, 2012.
64. Skoog I, Wallin A, Fredman P, Hesse C, Aevarsson O, Karlsson I, Gottfries CG, Blennow K. A population study on blood-brain barrier function in 85-year-olds: relation to Alzheimer's disease and vascular dementia. Neurology 50: 966-971, 1998.
65. Smith EE, Greenberg SM. Beta-amyloid, blood vessels and brain function. Stroke 40: 2601-2606, 2009.
66. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, De la Monte SM. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - is this type 3 diabetes? J Alzheimers Dis 7: 63-80, 2005.
67. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Burki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 94: 13287-13292, 1997.
68. Tamaki C, Ohtsuki S, Terasaki T. Insulin facilitates the hepatic clearance of plasma amyloid β-peptide (1-40) by intracellular translocation of low-density lipoprotein receptor-related protein 1 (LRP-1) to the plasma membrane in hepatocytes. Mol Pharmacol 72: 850-855, 2007.
69. Taylor AC, Seltz LM, Yates PA, Peirce SM. Chronic whole-body hypoxia induces intussusceptive angiogenesis and microvascular remodelling in the mouse retina. Microvasc Res 79: 93-101, 2010.
70. Vilsboll T, Zdravkovic M, Le-Thi T, Krarup T, Schmitz O, Courreges JP, Verhoeven R, Buganova I, Madsbad S. Liraglutide, a long-acting human glucagon-like peptide-1 analog, given as monotherapy significantly improves glycaemic control and lowers body weight without risk of hypoglycaemia in patients with type 2 diabetes. Diabetes Care 30: 1608-1610, 2007.
71. Vinters HV, Wang ZZ, Secor DL. Brain parenchymal and microvascular amyloid in Alzheimer's disease. Brain Pathol 6: 179-195, 1996.
72. Walker EJ, Shen F, Young WL, Su H. Cerebrovascular casting of the adult mouse for 3D imaging and morphological analysis. J Vis Exp 57: e2958, 2011.
73. Wang Y, Liu J, Zhang Z, Wang X, Zhang C. Structure and permeability changes of the blood-brain barrier in APP/PS1 mice: an Alzheimer's disease animal model. Neurochem J 5: 220-222, 2011.
74. Wei Y, Mojsov S. Tissue-specific expression of the human receptor for glucagon-like peptide-1: brain, heart and pancreatic forms have the same deduced amino acid sequences. FEBS Lett 358: 219-224, 1995.
75. Weiner DE, Bartolomei K, Scott T, Price LL, Griffith JL, Rosenberg I, Levey AS, Folstein MF, Sarnak MJ. Albuminuria, cognitive functioning, and white matter hyperintensities in homebound elders. Am J Kidney Dis 53: 438-447, 2009.
76. Weller RO, Boche D, Nicoll JAR. Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 118: 87-102, 2009.
77. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO. Perivascular drainage of amyloid-β peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 18: 253-266, 2008.
78. swe/PS1dE9) of Alzheimer's disease. Neurosci Bull 27: 221-232, 2011.