Disturbed cross talk between insulin-like growth factor I and AMP-activated protein kinase as a possible cause of vascular dysfunction in the amyloid precursor protein/presenilin 2 mouse model of Alzheimer's disease

Journal of Neuroscience

Volumn 27, Issue 4, 2007, Pages 824-831

  Lopez Lopez, Cristina ^a,b   Dietrich, Marcelo O ^a   Metzger, Friedrich ^b   Loetscher, Hansruedi ^b   Torres Aleman, Ignacio ^a  

^a INSTITUTO CAJAL   (Spain)

^b Preclinical Research   (Switzerland)

Author keywords

Alzheimer's disease; AMPK; Brain endothelial cells; Insulin like growth factor I; Intracellular signaling; Vascular endothelial growth factor

Indexed keywords

ADENOSINE PHOSPHATE; AMYLOID PRECURSOR PROTEIN; PRESENILIN 2; PROTEIN KINASE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; VASCULOTROPIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD VESSEL; CELL DIVISION; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; VASCULAR DISEASE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MULTIENZYME COMPLEXES; PRESENILIN-2; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; VASCULAR DISEASES;

EID: 33846590099     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4345-06.2007     Document Type: Article

References (55)

1. Almeida A, Cidad P, Delgado-Esteban M, Fernandez E, Garcia-Nogales P, Bolanos JP (2005) Inhibition of mitochondrial respiration by nitric oxide: its role in glucose metabolism and neuroprotection. J Neurosci Res 79:166-171.
2. Blum-Degen D, Frolich L, Hoyer S, Riederer P (1995) Altered regulation of brain glucose metabolism as a cause of neurodegenerative disorders? J Neural Transm Suppl 46:139-147.
3. Brera B, Serrano A, de Ceballos ML (2000) Beta-amyloid peptides are cytotoxic to astrocytes in culture: a role for oxidative stress. Neurobiol Dis 7:395-405.
4. Buee L, Hof PR, Bouras C, Delacourte A, Perl DP, Morrison JH, Fillit HM (1994) Pathological alterations of the cerebral microvasculature in Alzheimer's disease and related dementing disorders. Acta Neuropathol (Berl) 87:469-480.
5. Campbell M, Allen WE, Sawyer C, Vanhaesebroeck B, Trimble ER (2004) Glucose-potentiated chemotaxis in human vascular smooth muscle is dependent on cross-talk between the PI3K and MAPK signaling pathways. Circ Res 95:380-388.
6. Carling D (2004) The AMP-activated protein kinase cascade - a unifying system for energy control. Trends Biochem Sci 29:18-24.
7. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9:653-660.
8. Carrascosa C, Torres-Aleman I, Lopez-Lopez C, Carro E, Espejo L, Torrado S, Torrado JJ (2004) Microspheres containing insulin-like growth factor I for treatment of chronic neurodegeneration. Biomaterials 25:707-714.
9. Carro E, Torres-Aleman I (2004) The role of insulin and insulin-like growth factor I in the molecular and cellular mechanisms underlying the pathology of Alzheimer's disease. Eur J Pharmacol 490:127-133.
10. Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8:1390-1397.
11. Carro E, Spuch C, Trejo JL, Antequera D, Torres-Aleman I (2005) Choroid plexus megalin is involved in neuroprotection by serum insulin-like growth factor I. J Neurosci 25:10884-10893.
12. Carro E, Trejo JL, Gerber A, Loetscher H, Torrado J, Metzger F, Torres-Aleman I (2006a) Therapeutic actions of insulin-like growth factor I on APP/PS2 mice with severe brain amyloidosis. Neurobiol Aging 27:1250-1257.
13. Carro E, Trejo JL, Spuch C, Bohl D, Heard JM, Torres-Aleman I (2006b) Blockade of the insulin-like growth factor I receptor in the choroid plexus originates Alzheimer's-like neuropathology in rodents: new cues into the human disease? Neurobiol Aging 27:1618-1631.
14. Dagher Z, Ruderman N, Tornheim K, Ido Y (2001) Acute regulation of fatty acid oxidation and AMP-activated protein kinase in human umbilical vein endothelial cells. Circ Res 88:1276-1282.
15. Deane R, Wu Z, Sagare A, Davis J, Du YS, Hamm K, Xu F, Parisi M, LaRue B, Hu HW, Spijkers P, Guo H, Song X, Lenting PJ, Van Nostrand WE, Zlokovic BV (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43:333-344.
16. DeBosch BJ, Baur E, Deo BK, Hiraoka M, Kumagai AK (2001) Effects of insulin-like growth factor-1 on retinal endothelial cell glucose transport and proliferation. J Neurochem 77:1157-1167.
17. de la Torre JC (2000) Impaired cerebromicrovascular perfusion. Summary of evidence in support of its causality in Alzheimer's disease. Ann NY Acad Sci 924:136-152.
18. Fernandez AM, de la Vega AG, Torres-Aleman I (1998) Insulin-like growth factor I restores motor coordination in a rat model of cerebellar ataxia. Proc Natl Acad Sci USA 95:1253-1258.
19. Ferrara N (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 25:581-611.
20. Fryer LG, Foufelle F, Barnes K, Baldwin SA, Woods A, Carling D (2002) Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells. Biochem J 363:167-174.
21. Gasparini L, Xu H (2003) Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci 26:404-406.
22. Gonzalez I, Tripathi G, Carter EJ, Cobb LJ, Salih DA, Lovett FA, Holding C, Pell JM (2004) Akt2, a novel functional link between p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase pathways in myogenesis. Mol Cell Biol 24:3607-3622.
23. Grammas P, Yamada M, Zlokovic B (2002) The cerebromicrovasculature: a key player in the pathogenesis of Alzheimer's disease. J Alzheimers Dis 4:217-223.
24. Greenberg DA, Jin K (2005) From angiogenesis to neuropathology. Nature 438:954-959.
25. Hardie DG (2003) Minireview: The AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144:5179-5183.
26. Holt RI, Simpson HL, Sonksen PH (2003) The role of the growth hormone-insulin-like growth factor axis in glucose homeostasis. Diabet Med 20:3-15.
27. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5:347-360.
28. Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15-25.
29. Kefas BA, Heimberg H, Vaulont S, Meisse D, Hue L, Pipeleers D, Van de Casteele M (2003) AICA-riboside induces apoptosis of pancreatic beta cells through stimulation of AMP-activated protein kinase. Diabetologia 46:250-254.
30. Kim J, Yoon MY, Choi SL, Kang I, Kim SS, Kim YS, Choi YK, Ha J (2001) Effects of stimulation of AMP-activated protein kinase on insulin-like growth factor 1- and epidermal growth factor-dependent extracellular signal-regulated kinase pathway. J Biol Chem 276:19102-19110.
31. Lopez-Lopez C, LeRoith D, Torres-Aleman I (2004) Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci USA 101:9833-9838.
32. Mattson MP, Pedersen WA, Duan W, Culmsee C, Camandola S (1999) Cellular and molecular mechanisms underlying perturbed energy metabolism and neuronal degeneration in Alzheimer's and Parkinson's diseases. Ann NY Acad Sci 893:154-175.
33. Menze MA, Clavenna MJ, Hand SC (2005) Depression of cell metabolism and proliferation by membrane-permeable and -impermeable modulators: role for AMP-to-ATP ratio. Am J Physiol Regul Integr Comp Physiol 288:R501-R510.
34. Miao J, Xu F, Davis J, Otte-Holler I, Verbeek MM, Van Nostrand WE (2005) Cerebral microvascular amyloid beta protein deposition induces vascular degeneration and neuroinflammation in transgenic mice expressing human vasculotropic mutant amyloid beta precursor protein. Am J Pathol 167:505-515.
35. Nagata D, Mogi M, Walsh K (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem 278:31000-31006.
36. Ojuka EO (2004) Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc Nutr Soc 63:275-278.
37. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K (2004) Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 279:1304-1309.
38. Park L, Anrather J, Zhou P, Frys K, Pitstick R, Younkin S, Carlson GA, Iadecola C (2005) NADPH oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloid β peptide. J Neurosci 25:1769-1777.
39. Pons S, Torres-Aleman I (2000) Insulin-like growth factor-I stimulates dephosphorylation of Ikappa B through the serine phosphatase calcineurin (protein phosphatase 2B). J Biol Chem 275:38620-38625.
40. Reed MG, Howard CV (1998) Surface-weighted star volume: concept and estimation. J Microsc 190:350-356.
41. Richards JG, Higgins GA, Ouagazzal AM, Ozmen L, Kew JN, Bohrmann B, Malherbe P, Brockhaus M, Loetscher H, Czech C, Huber G, Bluethmann H, Jacobsen H, Kemp JA (2003) PS2APP transgenic mice, coexpressing hPS2mut and hAPPswe, show age-related cognitive deficits associated with discrete brain amyloid deposition and inflammation. J Neurosci 23:8989-9003.
42. Rivera EJ, Goldin A, Fulmer N, Tavares R, Wands JR, De La Monte SM (2005) Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J Alzheimers Dis 8:247-268.
43. Rosenkranz AR, Schmaldienst S, Stuhlmeier KM, Chen W, Knapp W, Zlabinger GJ (1992) A microplate assay for the detection of oxidative products using 2′,7′-dichlorofluorescin-diacetate. J Immunol Methods 156:39-45.
44. Ruderman NB, Cacicedo JM, Itani S, Yagihashi N, Saha AK, Ye JM, Chen K, Zou M, Carling D, Boden G, Cohen RA, Keaney J, Kraegen EW, Ido Y (2003) Malonyl-CoA and AMP-activated protein kinase (AMPK): possible links between insulin resistance in muscle and early endothelial cell damage in diabetes. Biochem Soc Trans 31:202-206.
45. Suzuki A, Kusakai G, Kishimoto A, Shimojo Y, Ogura T, Lavin MF, Esumi H (2004) IGF-1 phosphorylates AMPK-alpha subunit in ATM-dependent and LKB1-independent manner. Biochem Biophys Res Commun 324:986-992.
46. Tarkowski E, Issa R, Sjogren M, Wallin A, Blennow K, Tarkowski A, Kumar P (2002) Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol Aging 23:237-243.
47. Torres-Aleman I, Naftolin F, Robbins RJ (1990) Trophic effects of insulinlike growth factor-I on fetal rat hypothalamic cells in culture. Neuroscience 35:601-608.
48. Trejo JL, Carro E, Torres-Aleman I (2001) Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21:1628-1634.
49. von Kienlin M, Kunnecke B, Metzger F, Steiner G, Richards JG, Ozmen L, Jacobsen H, Loetscher H (2005) Altered metabolic profile in the frontal cortex of PS2APP transgenic mice, monitored throughout their life span. Neurobiol Dis 18:32-39.
50. Wang Z, Wang M, Carr BI (2005) Hepatocyte growth factor enhances protein phosphatase Cdc25A inhibitor compound 5-induced hepatoma cell growth inhibition via Akt-mediated MAPK pathway. J Cell Physiol 203:510-519.
51. Wiebel ER (1979) Stereological methods. Practical methods for biological morphometry. London: Academic.
52. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124.
53. Wu Z, Guo H, Chow N, Sallstrom J, Bell RD, Deane R, Brooks AI, Kanagala S, Rubio A, Sagare A, Liu D, Li F, Armstrong D, Gasiewicz T, Zidovetzki R, Song X, Hofman F, Zlokovic BV (2005) Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat Med 11:959-965.
54. Yun H, Lee M, Kim SS, Ha J (2005) Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J Biol Chem 280:9963-9972.
55. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA 99:15983-15987.