NDP-α-MSH induces intense neurogenesis and cognitive recovery in Alzheimer transgenic mice through activation of melanocortin MC4 receptors

Molecular and Cellular Neuroscience

Volumn 67, Issue , 2015, Pages 13-21

  Giuliani, Daniela ^a   Neri, Laura ^a   Canalini, Fabrizio ^a   Calevro, Anita ^a   Ottani, Alessandra ^a   Vandini, Eleonora ^a   Sena, Paola ^a   Zaffe, Davide ^a   Guarini, Salvatore ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Alzheimer's disease; Functional integration; Learning and memory; Melanocortin MC4 receptors; Neurogenesis; Tg2576 mice

Indexed keywords

ALPHA INTERMEDIN; BROXURIDINE; MELANIN CONCENTRATING HORMONE RECEPTOR 4 ANTAGONIST; MELANOCORTIN 4 RECEPTOR; PEPTIDE HORMONE RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; MSH, 4-NLE-7-PHE-ALPHA-;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN HISTOLOGY; CELL MATURATION; CELL MIGRATION; CELLULAR DISTRIBUTION; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFICACY; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MALE; MONOTHERAPY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; METABOLISM;

ANIMALIA; MUS; MUS MUSCULUS;

ALPHA-MSH; ALZHEIMER DISEASE; ANIMALS; COGNITION; HIPPOCAMPUS; MICE; NEUROGENESIS; RECEPTOR, MELANOCORTIN, TYPE 4;

EID: 84930656266     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2015.05.004     Document Type: Article

References (67)

1. Anderson B. Is alpha-MSH deficiency the cause of Alzheimer's disease?. Med. Hypotheses 1986, 19:379-385.
2. Arai H., Moroji T., Kosaka K., Iizuka R. Extrahypophyseal distribution of α-melanocyte stimulating hormone (α-MSH)-like immunoreactivity in postmortem brains from normal subjects and Alzheimer-type dementia patients. Brain Res. 1986, 377:305-310.
3. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8:963-970.
4. Bayer T.A., Wirths O. Focusing the amyloid cascade hypothesis on N-truncated Abeta peptides as drug targets against Alzheimer's disease. Acta Neuropathol. 2014, 127:787-801.
5. Becker M., Lavie V., Solomon B. Stimulation of endogenous neurogenesis by anti-EFRH immunization in a transgenic mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1691-1696.
6. Ben Menachem-Zidon O., Menahem Y.B., Hur T.B., Yirmiya R. Intra-hippocampal transplantation of neural precursor cells with transgenic over-expression of IL-1 receptor antagonist rescues memory and neurogenesis impairments in an Alzheimer's disease model. Neuropsychopharmacology 2014, 39:401-414.
7. Benarroch E.E. Adult neurogenesis in the dentate gyrus: general concepts and potential implications. Neurology 2013, 81:1443-1452.
8. Bharne A.P., Upadhya M.A., Kokare D.M., Subhedar N.K. Effect of alpha-melanocyte stimulating hormone on locomotor recovery following spinal cord injury in mice: role of serotonergic system. Neuropeptides 2011, 45:25-31.
9. Bitto A., Polito F., Irrera N., Calò M., Spaccapelo L., Marini H.R., Giuliani D., Ottani A., Rinaldi M., Minutoli L., Guarini S., Squadrito F., Altavilla D. Protective effects of melanocortins on short-term changes in a rat model of traumatic brain injury. Crit. Care Med. 2012, 40:945-951.
10. Blennow K. Biomarkers in Alzheimer's disease drug development. Nat. Med. 2010, 16:1218-1222.
11. Boekhoorn K., Joels M., Lucassen P.J. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol. Dis. 2006, 24:1-14.
12. Brzoska T., Luger T.A., Maaser C., Abel C., Böhm M. α-Melanocyte-stimulating hormone and related tripeptides: biochemistry, antiinflammatory and protective effects in vitro and in vivo, and future perspectives for the treatment of immune-mediated inflammatory diseases. Endocr. Rev. 2008, 29:581-602.
13. Caruso C., Carniglia L., Durand D., Gonzalez P.V., Scimonelli T.N., Lasaga M. Melanocortin 4 receptor activation induces brain-derived neurotrophic factor expression in rat astrocytes through cyclic AMP-protein kinase A pathway. Mol. Cell. Endocrinol. 2012, 348:47-54.
14. Caruso V., Lagerström M.C., Olszewski P.K., Fredriksson R., Schiöth H.B. Synaptic changes induced by melanocortin signalling. Nat. Rev. Neurosci. 2014, 15:98-110.
15. Catania A., Gatti S., Colombo G., Lipton J.M. Targeting melanocortin receptors as a novel strategy to control inflammation. Pharmacol. Rev. 2004, 56:1-29.
16. Chen G., Frøkiær J., Pedersen M., Nielsen S., Si Z., Pang Q., Stødkilde-Jørgensen H. Reduction of ischemic stroke in rat brain by alpha melanocyte stimulating hormone. Neuropeptides 2008, 42:331-338.
17. Corander M.P., Fenech M., Coll A.P. Science of self-preservation: how melanocortin action in the brain modulates body weight, blood pressure and ischemic damage. Circulation 2009, 120:2260-2268.
18. Facchinetti F., Nappi G., Petraglia F., Martignoni E., Sinforiani E., Genazzani A.R. Central ACTH deficit in degenerative and vascular dementia. Life Sci. 1984, 35:1691-1697.
19. Franco R., Cedazo-Minguez A. Successful therapies for Alzheimer's disease: why so many in animal models and none in humans?. Front. Pharmacol. 2014, 5:146.
20. Freiherr J., Hallschmid M., Frey W.H., Brünner Y.F., Chapman C.D., Hölscher C., Craft S., De Felice F.G., Benedict C. Intranasal insulin as a treatment for Alzheimer's disease: a review of basic research and clinical evidence. CNS Drugs 2013, 27:505-514.
21. Galimberti D., Ghezzi L., Scarpini E. Immunotherapy against amyloid pathology in Alzheimer's disease. J. Neurol. Sci. 2013, 333:50-54.
22. Gatti S., Lonati C., Acerbi F., Sordi A., Leonardi P., Carlin A., Gaini S.M., Catania A. Protective action of NDP-MSH in experimental subarachnoid hemorrhage. Exp. Neurol. 2012, 234:230-238.
23. 7]α-melanocyte-stimulating hormone for long-lasting protection against ischemic stroke, in Mongolian gerbils. Eur. J. Pharmacol. 2006, 538:48-56.
24. Giuliani D., Mioni C., Altavilla D., Leone S., Bazzani C., Minutoli L., Bitto A., Cainazzo M.M., Marini H., Zaffe D., Botticelli A.R., Pizzala R., Savio M., Necchi D., Schiöth H.B., Bertolini A., Squadrito F., Guarini S. Both early and delayed treatment with melanocortin 4 receptor-stimulating melanocortins produces neuroprotection in cerebral ischemia. Endocrinology 2006, 147:1126-1135.
25. Giuliani D., Ottani A., Mioni C., Bazzani C., Galantucci M., Minutoli L., Bitto A., Zaffe D., Botticelli A.R., Squadrito F., Guarini S. Neuroprotection in focal cerebral ischemia owing to delayed treatment with melanocortins. Eur. J. Pharmacol. 2007, 570:57-65.
26. Giuliani D., Ottani A., Minutoli L., Di Stefano V., Galantucci M., Bitto A., Zaffe D., Altavilla D., Botticelli A.R., Squadrito F., Guarini S. Functional recovery after delayed treatment of ischemic stroke with melanocortins is associated with overexpression of the activity-dependent gene Zif268. Brain Behav. Immun. 2009, 23:844-850.
27. 4 receptors induces marked neurogenesis and long-lasting functional recovery. Acta Neuropathol. 2011, 122:443-453.
28. Giuliani D., Minutoli L., Ottani A., Spaccapelo L., Bitto A., Galantucci M., Altavilla D., Squadrito F., Guarini S. Melanocortins as potential therapeutic agents in severe hypoxic conditions. Front. Neuroendocrinol. 2012, 33:179-193.
29. Giuliani D., Ottani A., Zaffe D., Galantucci M., Strinati F., Lodi R., Guarini S. Hydrogen sulfide slows down progression of experimental Alzheimer's disease by targeting multiple pathophysiological mechanisms. Neurobiol. Learn. Mem. 2013, 104:82-91.
30. Giuliani D., Bitto A., Galantucci M., Zaffe D., Ottani A., Irrera N., Neri L., Cavallini G.M., Altavilla D., Botticelli A.R., Squadrito F., Guarini S. Melanocortins protect against progression of Alzheimer's disease in triple-transgenic mice by targeting multiple pathophysiological pathways. Neurobiol. Aging 2014, 35:537-547.
31. Giuliani D., Galantucci M., Neri L., Canalini F., Calevro A., Bitto A., Ottani A., Vandini E., Sena P., Sandrini M., Squadrito F., Zaffe D., Guarini S. Melanocortins protect against brain damage and counteract cognitive decline in a transgenic mouse model of moderate Alzheimer's disease. Eur. J. Pharmacol. 2014, 740:144-150.
32. Glat M.J., Offen D. Cell and gene therapy in Alzheimer's disease. Stem Cells Dev. 2013, 22:1490-1496.
33. Guarini S., Bazzani C., Mattera Ricigliano G., Bini A., Tomasi A., Bertolini A. Influence of ACTH-(1-24) on free radical levels in the blood of haemorrhage-shocked rats: direct ex vivo detection by electron spin resonance spectrometry. Br. J. Pharmacol. 1996, 119:29-34.
34. Guarini S., Bini A., Bazzani C., Mattera Ricigliano G., Cainazzo M.M., Tomasi A., Bertolini A. Adrenocorticotropin normalizes the blood levels of nitric oxide in hemorrhage-shocked rats. Eur. J. Pharmacol. 1997, 336:15-21.
35. Gustavsson A., Svensson M., Jacobi F., Allgulander C., Alonso J., Beghi E., Dodel R., Ekman M., Faravelli C., Fratiglioni L., Gannon B., Jones D.H., Jennum P., Jordanova A., Jönsson L., Karampampa K., Knapp M., Kobelt G., Kurth T., Lieb R., Linde M., Ljungcrantz C., Maercker A., Melin B., Moscarelli M., Musayev A., Norwood F., Preisig M., Pugliatti M., Rehm J., Salvador-Carulla L., Schlehofer B., Simon R., Steinhausen H.C., Stovner L.J., Vallat J.M., Van den Bergh P., Van Os J., Vos P., Xu W., Wittchen H.U., Jönsson B., Olesen J., CDBE2010Study Group Cost of disorders of the brain in Europe 2010. Eur. Neuropsychopharmacol. 2011, 21:718-779.
36. Holloway P.M., Smith H.K., Renshaw D., Flower R.J., Getting S.J., Gavins F.N.E. Targeting the melanocortin receptor system for anti-stroke therapy. Trends Pharmacol. Sci. 2011, 32:90-98.
37. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
38. Iqbal K., Grundke-Iqbal I. Alzheimer's disease, a multifactorial disorder seeking multitherapies. Alzheimers Dement. 2010, 6:420-424.
39. Iqbal K., Grundke-Iqbal I. Opportunities and challenges in developing Alzheimer disease therapeutics. Acta Neuropathol. 2011, 122:543-549.
40. Ittner L.M., Götz J. Amyloid-β and tau - a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 2011, 12:65-72.
41. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:343-347.
42. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci. 2010, 33:569-579.
43. Lichtenwalner R.J., Parent J.M. Adult neurogenesis and the ischemic forebrain. J. Cereb. Blood Flow Metab. 2006, 26:1-20.
44. Lilja A.M., Röjdner J., Mustafiz T., Thomé C.M., Storelli E., Gonzalez D., Unger-Lithner C., Greig N.H., Nordberg A., Marutle A. Age-dependent neuroplasticity mechanisms in Alzheimer Tg2576 mice following modulation of brain amyloid-β levels. PLoS ONE 2013, 8:e58752.
45. Marlatt M.W., Lucassen P.J. Neurogenesis and Alzheimer's disease: biology and pathophysiology in mice and men. Curr. Alzheimer Res. 2010, 7:113-125.
46. Marlatt M.W., Potter M.C., Bayer T.A., van Praag H., Lucassen P.J. Prolonged running, not fluoxetine treatment, increases neurogenesis, but does not alter neuropathology, in the 3xTg mouse model of Alzheimer's disease. Curr. Top. Behav. Neurosci. 2013, 15:313-340.
47. Minutoli L., Squadrito F., Nicotina P.A., Giuliani D., Ottani A., Polito F. Melanocortin 4 receptor stimulation decreases pancreatitis severity in rats by activation of the cholinergic anti-inflammatory pathway. Crit. Care Med. 2011, 39:1089-1096.
48. 3 receptors. Eur. J. Pharmacol. 2003, 477:227-234.
49. Mountjoy K.G. Distribution and function of melanocortin receptors within the brain. Adv. Exp. Med. Biol. 2010, 681:29-48.
50. Mu Y., Gage F.H. Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol. Neurodegener. 2011, 6:85.
51. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Aβ and synaptic dysfunction. Neuron 2003, 39:409-421.
52. Perry E.K., Johnson M., Ekonomou A., Perry R.H., Ballard C., Attems J. Neurogenic abnormalities in Alzheimer's disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol. Dis. 2012, 47:155-162.
53. Rainero I., May C., Kaye J.A., Friedland R.P., Rapoport S.I. CSF α-MSH in dementia of the Alzheimer type. Neurology 1988, 38:1281-1284.
54. Salloway S., Sperling R., Fox N.C., Blennow K., Klunk W., Raskind M., Sabbagh M., Honig L.S., Porsteinsson A.P., Ferris S., Reichert M., Ketter N., Nejadnik B., Guenzler V., Miloslavsky M., Wang D., Lu Y., Lull J., Tudor I.C., Liu E., Grundman M., Yuen E., Black R., Brashear H.R., Bapineuzumab 301 and 302 Clinical Trial Investigators Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 2014, 370:322-333.
55. Shen Y., Fu W.Y., Cheng E.Y., Fu A.K., Ip N.Y. Melanocortin-4 receptor regulates hippocampal synaptic plasticity through a protein kinase A-dependent mechanism. J. Neurosci. 2013, 33:464-472.
56. 4 receptor agonists counteract late inflammatory and apoptotic responses and improve neuronal functionality after cerebral ischemia. Eur. J. Pharmacol. 2011, 670:479-486.
57. Spaccapelo L., Galantucci M., Neri L., Contri M., Pizzala R., D'Amico R., Ottani A., Sandrini M., Zaffe D., Giuliani D., Guarini S. Up-regulation of the canonical Wnt-3A and Sonic hedgehog signaling underlies melanocortin-induced neurogenesis after cerebral ischemia. Eur. J. Pharmacol. 2013, 707:78-86.
58. Sperling R.A., Karlawish J., Johnson K.A. Preclinical Alzheimer disease - the challenges ahead. Nat. Rev. Neurol. 2013, 9:54-58.
59. Suh H., Deng W., Gage F.H. Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 2009, 25:253-275.
60. Sun Y., Ji K., Xie L., Childs J., Mao X.O., Logvinova A., Greenberg D.A. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 2003, 111:1843-1851.
61. Tashiro A., Makino H., Gage F.H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 2007, 27:3252-3259.
62. Taupin P. Neurogenesis, NSCs, pathogenesis and therapies for Alzheimer's disease. Front. Biosci. (Schol. Ed.) 2011, 3:178-190.
63. Tayeb H.O., Yang H.D., Price B.H., Tarazi F.I. Pharmacotherapies for Alzheimer's disease: beyond cholinesterase inhibitors. Pharmacol. Ther. 2012, 134:8-25.
64. Veyrac A., Gros A., Bruel-Jungerman E., Rochefort C., Kleine Borgmann F.B., Jessberger S., Laroche S. Zif268/egr1 gene controls the selection, maturation and functional integration of adult hippocampal newborn neurons by learning. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7062-7067.
65. Wang L., Zhang Z., Wang Y., Zhang R., Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004, 35:1732-1737.
66. Wang J.M., Singh C., Liu L., Irwin R.W., Chen S., Chung E.J., Thompson R.F., Brinton R.D. Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6498-6503.
67. Wikberg J.E., Mutulis F. Targeting melanocortin receptors: an approach to treat weight disorders and sexual dysfunction. Nat. Rev. Drug Discov. 2008, 7:307-323.