Intranasal "painless" human nerve growth factors slows amyloid neurodegeneration and prevents memory deficits in app x PS1 mice

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Capsoni, Simona ^a,b   Marinelli, Sara ^c   Ceci, Marcello ^a   Vignone, Domenico ^a   Amato, Gianluca ^a   Malerba, Francesca ^a,b   Paoletti, Francesca ^a   Meli, Giovanni ^a   Viegi, Alessandro ^b   Pavone, Flaminia ^c   Cattaneo, Antonino ^a,b  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; HUMAN NERVE GROWTH FACTOR; NERVE GROWTH FACTOR; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPROTECTIVE AGENT; PHOSPHOLIPASE C GAMMA; PROTEIN TYROSINE KINASE A; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DRUG ACTIVITY; GENE DELIVERY SYSTEM; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE DEGENERATION; NEUROPATHY; NOCICEPTION; NONHUMAN; RAT; RECEPTOR BINDING; ALZHEIMER DISEASE; ANIMAL; ANIMAL BEHAVIOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL STRUCTURE; DISEASE COURSE; DRUG EFFECT; GENETICS; HUMAN; INTRANASAL DRUG ADMINISTRATION; LEARNING; MALE; MEMORY DISORDER; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MUS;

ADMINISTRATION, INTRANASAL; ALZHEIMER DISEASE; AMYLOID; ANIMALS; BEHAVIOR, ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DISEASE PROGRESSION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEARNING; MALE; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTATION; NERVE GROWTH FACTOR; NEURODEGENERATIVE DISEASES; NEURONS; NEUROPROTECTIVE AGENTS; NOCICEPTION; PHOSPHOLIPASE C GAMMA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR, TRKA; SIGNAL TRANSDUCTION; SYNAPTOPHYSIN;

EID: 84861614275     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037555     Document Type: Article

References (74)

1. Levi-Montalcini R, (1987) The nerve growth factor 35 years later. Science 237: 1154-1162.
2. Delcroix JD, Valletta J, Wu C, Howe CL, Lai CF, et al. (2004) Trafficking the NGF signal: implications for normal and degenerating neurons. Prog Brain Res 146: 3-23.
3. Tuszynski MH, (2007) Nerve growth factor gene therapy in Alzheimer disease. Alzheimer Dis Assoc Disord 21: 179-189.
4. Mufson EJ, Counts SE, Perez SE, Ginsberg SD, (2008) Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 8: 1703-1718.
5. Chao MV, Rajagopal R, Lee FS, (2006) Neurotrophin signalling in health and disease. Clin Sci (Lond) 110: 167-173.
6. Giacobini E, Becker RE, (2007) One hundred years after the discovery of Alzheimer's disease. A turning point for therapy? J Alzheimers Dis 12: 37-52.
7. Cattaneo A, Capsoni S, Paoletti F, (2008) Towards non invasive Nerve Growth Factor therapies for Alzheimer's disease. Journal of Alzheimer's disease 15: 255-283.
8. Matrone C, Ciotti MT, Mercanti D, Marolda R, Calissano P, (2008) NGF and BDNF signaling control amyloidogenic route and Abeta production in hippocampal neurons. Proc Natl Acad Sci U S A 105: 13139-13144.
9. Thoenen H, Sendtner M, (2002) Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nat Neurosci 5 Supplpp. 1046-1050.
10. Poduslo JF, Curran GL, Berg CT, (1994) Macromolecular permeability across the blood-nerve and blood-brain barriers. Proc Natl Acad Sci U S A 91: 5705-5709.
11. Petty BG, Cornblath DR, Adornato BT, Chaudhry V, Flexner C, et al. (1994) The effect of systemically administered recombinant human nerve growth factor in healthy human subjects. Ann Neurol 36: 244-246.
12. Pezet S, McMahon SB, (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538.
13. Eriksdotter Jonhagen M, Nordberg A, Amberla K, Backman L, Ebendal T, et al. (1998) Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement Geriatr Cogn Disord 9: 246-257.
14. Tuszynski MH, Thal L, Pay M, Salmon DP, U HS, et al. (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11: 551-555.
15. Mandel RJ, (2010) CERE-110, an adeno-associated virus-based gene delivery vector expressing human nerve growth factor for the treatment of Alzheimer's disease. Curr Opin Mol Ther 12: 240-247.
16. Malerba F, Paoletti F, Capsoni S, Cattaneo A, (2011) Intranasal delivery of therapeutic proteins for neurological diseases. Expert Opin Drug Deliv 8: 1-20.
17. Frey IW, Liu J, Chen XQ, Thorne RG, Fawcett JR, et al. (1997) Delivery of 125I-NGF to the brain via the olfactory route. Drug Delivery 4: 87-92.
18. Capsoni S, Giannotta S, Cattaneo A, (2002) Nerve growth factor and galantamine ameliorate early signs of neurodegeneration in anti-nerve growth factor mice. Proc Natl Acad Sci U S A 99: 12432-12437.
19. Capsoni S, Covaceuszach S, Ugolini G, Spirito F, Vignone D, et al. (2009) Delivery of NGF to the Brain: Intranasal versus Ocular Administration in Anti-NGF Transgenic Mice. J Alzheimers Dis 16: 371-388.
20. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, et al. (2005) Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci U S A 102: 3811-3816.
21. Capsoni S, Covaceuszach S, Marinelli S, Ceci M, Bernardo A, et al. (2011) Taking Pain Out of NGF: A "Painless" NGF Mutant, Linked to Hereditary Sensory Autonomic Neuropathy Type V, with Full Neurotrophic Activity. PLoS One 6: e17321.
22. Einarsdottir E, Carlsson A, Minde J, Toolanen G, Svensson O, et al. (2004) A mutation in the nerve growth factor beta gene (NGFB) causes loss of pain perception. Hum Mol Genet 13: 799-805.
23. de Andrade DC, Baudic S, Attal N, Rodrigues CL, Caramelli P, et al. (2008) Beyond neuropathy in hereditary sensory and autonomic neuropathy type V: cognitive evaluation. Eur J Neurol 15: 712-719.
24. Covaceuszach S, Capsoni S, Marinelli S, Pavone F, Ceci M, et al. (2010) In vitro receptor binding properties of a "painless" NGF mutein, linked to hereditary sensory autonomic neuropathy type V. Biochem Biophys Res Commun 391: 824-829.
25. Covaceuszach S, Capsoni S, Ugolini G, Spirito F, Vignone D, et al. (2009) Development of a non invasive NGF-based therapy for Alzheimer's disease. Curr Alzheimer Res 6: 158-170.
26. Doya H, Ohtori S, Fujitani M, Saito T, Hata K, et al. (2005) c-Jun N-terminal kinase activation in dorsal root ganglion contributes to pain hypersensitivity. Biochem Biophys Res Commun 335: 132-138.
27. Malik-Hall M, Dina OA, Levine JD, (2005) Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J Neurosci 21: 3387-3394.
28. Reichardt LF, (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361: 1545-1564.
29. Chevalier S, Praloran V, Smith C, MacGrogan D, Ip NY, et al. (1994) Expression and functionality of the trkA proto-oncogene product/NGF receptor in undifferentiated hematopoietic cells. Blood 83: 1479-1485.
30. Barde YA, Edgar D, Thoenen H, (1980) Sensory neurons in culture: changing requirements for survival factors during embryonic development. Proc Natl Acad Sci U S A 77: 1199-1203.
31. Poluha W, Poluha DK, Ross AH, (1995) TrkA neurogenic receptor regulates differentiation of neuroblastoma cells. Oncogene 10: 185-189.
32. Sonnenfeld KH, Ishii DN, (1982) Nerve growth factor effects and receptors in cultured human neuroblastoma cell lines. J Neurosci Res 8: 375-391.
33. McMahon SB, Bennett DL, Priestley JV, Shelton DL, (1995) The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nat Med 1: 774-780.
34. Wilson SG, Smith SB, Chesler EJ, Melton KA, Haas JJ, et al. (2003) The heritability of antinociception: common pharmacogenetic mediation of five neurochemically distinct analgesics. J Pharmacol Exp Ther 304: 547-559.
35. Mogil JS, Miermeister F, Seifert F, Strasburg K, Zimmermann K, et al. (2005) Variable sensitivity to noxious heat is mediated by differential expression of the CGRP gene. Proc Natl Acad Sci U S A 102: 12938-12943.
36. Capsoni S, Ugolini G, Comparini A, Ruberti F, Berardi N, et al. (2000) Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice. Proc Natl Acad Sci U S A 97: 6826-6831.
37. Ruberti F, Capsoni S, Comparini A, Di Daniel E, Franzot J, et al. (2000) Phenotypic knockout of nerve growth factor in adult transgenic mice reveals severe deficits in basal forebrain cholinergic neurons, cell death in the spleen, and skeletal muscle dystrophy. J Neurosci 20: 2589-2601.
38. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, et al. (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19: 939-945.
39. Heikkinen T, Kalesnykas G, Rissanen A, Tapiola T, Iivonen S, et al. (2004) Estrogen treatment improves spatial learning in APP+PS1 mice but does not affect beta amyloid accumulation and plaque formation. Exp Neurol 187: 105-117.
40. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489.
41. Meli G, Visintin M, Cannistraci I, Cattaneo A, (2009) Direct in vivo intracellular selection of conformation-sensitive antibody domains targeting Alzheimer's amyloid-beta oligomers. J Mol Biol 387: 584-606.
42. Oderfeld-Nowak B, Orzylowska-Sliwinska O, Soltys Z, Zaremba M, Januszewski S, et al. (2003) Concomitant up-regulation of astroglial high and low affinity nerve growth factor receptors in the CA1 hippocampal area following global transient cerebral ischemia in rat. Neuroscience 120: 31-40.
43. Chong YH, Shin YJ, Lee EO, Kayed R, Glabe CG, et al. (2006) ERK1/2 activation mediates Abeta oligomer-induced neurotoxicity via caspase-3 activation and tau cleavage in rat organotypic hippocampal slice cultures. J Biol Chem 281: 20315-20325.
44. Mazzitelli S, Xu P, Ferrer I, Davis RJ, Tournier C, (2011) The Loss of c-Jun N-Terminal Protein Kinase Activity Prevents the Amyloidogenic Cleavage of Amyloid Precursor Protein and the Formation of Amyloid Plaques In Vivo. J Neurosci 31: 16969-16976.
45. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539.
46. Apfel SC, (2002) Nerve growth factor for the treatment of diabetic neuropathy: what went wrong, what went right, and what does the future hold? Int Rev Neurobiol 50: 393-413.
47. Mahapatra S, Mehta H, Woo SB, Neet KE, (2009) Identification of critical residues within the conserved and specificity patches of nerve growth factor leading to survival or differentiation. J Biol Chem 284: 33600-33613.
48. Aboulkassim T, Tong XK, Chung Tse Y, Wong TP, Woo SB, et al. (2011) Ligand-dependent TrkA activity in brain differentially affects spatial learning and long-term memory. Mol Pharmacol 80: 498-508.
49. He XL, Garcia KC, (2004) Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304: 870-875.
50. Wiesmann C, Ultsch MH, Bass SH, de Vos AM, (1999) Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor. Nature 401: 184-188.
51. Wehrman T, He X, Raab B, Dukipatti A, Blau H, et al. (2007) Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53: 25-38.
52. Holland DR, Cousens LS, Meng W, Matthews BW, (1994) Nerve growth factor in different crystal forms displays structural flexibility and reveals zinc binding sites. J Mol Biol 239: 385-400.
53. McDonald NQ, Lapatto R, Murray-Rust J, Gunning J, Wlodawer A, et al. (1991) New protein fold revealed by a 2.3-A resolution crystal structure of nerve growth factor. Nature 354: 411-414.
54. Heese K, Hock C, Otten U, (1998) Inflammatory signals induce neurotrophin expression in human microglial cells. J Neurochem 70: 699-707.
55. Junier MP, Suzuki F, Onteniente B, Peschanski M, (1994) Target-deprived CNS neurons express the NGF gene while reactive glia around their axonal terminals contain low and high affinity NGF receptors. Brain Res Mol Brain Res 24: 247-260.
56. Wang Y, Hagel C, Hamel W, Muller S, Kluwe L, et al. (1998) Trk A, B, and C are commonly expressed in human astrocytes and astrocytic gliomas but not by human oligodendrocytes and oligodendroglioma. Acta Neuropathol 96: 357-364.
57. Aguado F, Ballabriga J, Pozas E, Ferrer I, (1998) TrkA immunoreactivity in reactive astrocytes in human neurodegenerative diseases and colchicine-treated rats. Acta Neuropathol 96: 495-501.
58. Connor B, Young D, Lawlor P, Gai W, Waldvogel H, et al. (1996) Trk receptor alterations in Alzheimer's disease. Brain Res Mol Brain Res 42: 1-17.
59. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, et al. (2003) Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9: 453-457.
60. Wegiel J, Wang KC, Tarnawski M, Lach B, (2000) Microglia cells are the driving force in fibrillar plaque formation, whereas astrocytes are a leading factor in plague degradation. Acta Neuropathol 100: 356-364.
61. Jimenez S, Torres M, Vizuete M, Sanchez-Varo R, Sanchez-Mejias E, et al. (2011) Age-dependent accumulation of soluble amyloid beta (Abeta) oligomers reverses the neuroprotective effect of soluble amyloid precursor protein-alpha (sAPP(alpha)) by modulating phosphatidylinositol 3-kinase (PI3K)/Akt-GSK-3beta pathway in Alzheimer mouse model. J Biol Chem 286: 18414-18425.
62. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, et al. (2011) Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 31: 6627-6638.
63. Young KF, Pasternak SH, Rylett RJ, (2009) Oligomeric aggregates of amyloid beta peptide 1-42 activate ERK/MAPK in SH-SY5Y cells via the alpha7 nicotinic receptor. Neurochem Int 55: 796-801.
64. Nizzari M, Venezia V, Repetto E, Caorsi V, Magrassi R, et al. (2007) Amyloid precursor protein and Presenilin1 interact with the adaptor GRB2 and modulate ERK 1,2 signaling. J Biol Chem 282: 13833-13844.
65. Mehan S, Meena H, Sharma D, Sankhla R, (2011) JNK: a stress-activated protein kinase therapeutic strategies and involvement in Alzheimer's and various neurodegenerative abnormalities. J Mol Neurosci 43: 376-390.
66. Ma QL, Harris-White ME, Ubeda OJ, Simmons M, Beech W, et al. (2007) Evidence of Abeta- and transgene-dependent defects in ERK-CREB signaling in Alzheimer's models. J Neurochem 103: 1594-1607.
67. Bruno MA, Leon WC, Fragoso G, Mushynski WE, Almazan G, et al. (2009) Amyloid beta-induced nerve growth factor dysmetabolism in Alzheimer disease. J Neuropathol Exp Neurol 68: 857-869.
68. Capsoni S, Tiveron C, Vignone D, Amato G, Cattaneo A, (2010) Dissecting the involvement of tropomyosin-related kinase A and p75 neurotrophin receptor signaling in NGF deficit-induced neurodegeneration. Proc Natl Acad Sci U S A 107: 12299-12304.
69. Salehi A, Delcroix JD, Belichenko PV, Zhan K, Wu C, et al. (2006) Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 51: 29-42.
70. Houeland G, Romani A, Marchetti C, Amato G, Capsoni S, et al. (2010) Transgenic Mice with Chronic NGF Deprivation and Alzheimer's Disease-Like Pathology Display Hippocampal Region-Specific Impairments in Short- and Long-Term Plasticities. Journal of Neuroscience 30: 13089-13094.
71. Greene LA, Tischler AS, (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73: 2424-2428.
72. Culmsee C, Gerling N, Lehmann M, Nikolova-Karakashian M, Prehn JH, et al. (2002) Nerve growth factor survival signaling in cultured hippocampal neurons is mediated through TrkA and requires the common neurotrophin receptor P75. Neuroscience 115: 1089-1108.
73. Cattaneo A, Rapposelli B, Calissano P, (1988) Three distinct types of monoclonal antibodies after long-term immunization of rats with mouse nerve growth factor. J Neurochem 50: 1003-1010.
74. Capsoni S, Giannotta S, Cattaneo A, (2002) Beta-amyloid plaques in a model for sporadic Alzheimer's disease based on transgenic anti-nerve growth factor antibodies. Mol Cell Neurosci 21: 15-28.