Chronic administration of AMD3100 increases survival and alleviates pathology in SOD1G93A mice model of ALS

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Rabinovich Nikitin, Inna ^a   Ezra, Assaf ^a   Barbiro, Beka ^a   Rabinovich Toidman, Polina ^a   Solomon, Beka ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

ALS; AMD3100; Blood spinal cord barrier; CXCR4 CXCL12; Hematopoietic stem and progenitor cells; Microglia; SOD1G93A mice

Indexed keywords

CD36 ANTIGEN; CLAUDIN 5; INTERLEUKIN 6; OCCLUDIN; PLERIXAFOR; PROTEIN ZO1; TUMOR NECROSIS FACTOR ALPHA; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; CCL2 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CXCR4; CXCR4 PROTEIN, MOUSE; CYTOKINE; HETEROCYCLIC COMPOUND; MONOCYTE CHEMOTACTIC PROTEIN 1; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE; TJP1 PROTEIN, MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; FEMALE; LIFE EXTENSION; LONG TERM CARE; LUMBAR SPINAL CORD; MALE; MICROGLIA; MOTOR PERFORMANCE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SPINAL CORD MOTONEURON; SURVIVAL RATE; WEIGHT REDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOTONEURON; MUSCLE STRENGTH; PATHOLOGY; PSYCHOMOTOR DISORDERS; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CALCIUM-BINDING PROTEINS; CHEMOKINE CCL2; CLAUDIN-5; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MOTOR NEURONS; MUSCLE STRENGTH; PSYCHOMOTOR DISORDERS; RECEPTORS, CXCR4; SUPEROXIDE DISMUTASE; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84973293592     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0587-6     Document Type: Article

References (49)

1. Leigh PN. Chapter 13 Amyotrophic lateral sclerosis. Handb Clin Neurol. 2007;82:249-78.
2. Appel SH, Zhao W, Beers DR, Henkel JS. The microglial-motoneuron dialogue in ALS. Acta Myol. 2011;30:4-8.
3. Brites D, Vaz AR. Microglia centered pathogenesis in ALS: insights in cell interconnectivity. Front Cell Neurosci. 2014;8:117.
4. Sargsyan SA, Monk PN, Shaw PJ. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia. 2005;51:241-53.
5. West M, Mhatre M, Ceballos A, Floyd RA, Grammas P, Gabbita SP, Hamdheydari L, Mai T, Mou S, Pye QN, Stewart C, West S, Williamson KS, Zemlan F, Hensley K. The arachidonic acid 5-lipoxygenase inhibitor nordihydroguaiaretic acid inhibits tumor necrosis factor alpha activation of microglia and extends survival of G93A-SOD1 transgenic mice. J Neurochem. 2004;91:133-43.
6. Tikka TM, Vartiainen NE, Goldsteins G, Oja SS, Andersen PM, Marklund SL, Koistinaho J. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain. 2002;125(Pt 4):722-31.
7. Mizuno T, Kurotani T, Komatsu Y, Kawanokuchi J, Kato H, Mitsuma N, Suzumura A. Neuroprotective role of phosphodiesterase inhibitor ibudilast on neuronal cell death induced by activated microglia. Neuropharmacology. 2004;46:404-11.
8. Nikodemova M, Small AL, Smith SMC, Mitchell GS, Watters JJ. Spinal but not cortical microglia acquire an atypical phenotype with high VEGF, galectin-3 and osteopontin, and blunted inflammatory responses in ALS rats. Neurobiol Dis. 2014;69:43-53.
9. Roberts K, Zeineddine R, Corcoran L, Li W, Campbell IL, Yerbury JJ. Extracellular aggregated Cu/Zn superoxide dismutase activates microglia to give a cytotoxic phenotype. Glia. 2013;61:409-19.
10. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006;312:1389-92.
11. Kim Y-J, Park H-J, Lee G, Bang OY, Ahn YH, Joe E, Kim HO, Lee PH. Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action. Glia. 2009;57:13-23.
12. Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, Shioda S, Prockop DJ. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A. 2008;105:14638-43.
13. Sheikh AM, Nagai A, Wakabayashi K, Narantuya D, Kobayashi S, Yamaguchi S, Kim SU. Mesenchymal stem cell transplantation modulates neuroinflammation in focal cerebral ischemia: contribution of fractalkine and IL-5. Neurobiol Dis. 2011;41:717-24.
14. Ripoll CB, Flaat M, Klopf-Eiermann J, Fisher-Perkins JM, Trygg CB, Scruggs BA, McCants ML, Leonard HP, Lin AF, Zhang S, Eagle ME, Alvarez X, Li YT, Li SC, Gimble JM, Bunnell BA. Mesenchymal lineage stem cells have pronounced anti-inflammatory effects in the twitcher mouse model of Krabbe's disease. Stem Cells. 2011;29:67-77.
15. Vercelli A, Mereuta OM, Garbossa D, Muraca G, Mareschi K, Rustichelli D, Ferrero I, Mazzini L, Madon E, Fagioli F. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis. 2008;31:395-405.
16. Shin J-W, Lee JK, Lee JE, Min W-K, Schuchman EH, Jin HK, Bae J-S. Combined effects of hematopoietic progenitor cell mobilization from bone marrow by granulocyte colony stimulating factor and AMD3100 and chemotaxis into the brain using stromal cell-derived factor-1α in an Alzheimer's disease mouse model. Stem Cells. 2011;29:1075-89.
17. Tran PB, Miller RJ. Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci. 2003;4:444-55.
18. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci. 2001;4:702-10.
19. De Clercq E. The AMD3100 story: the path to the discovery of a stem cell mobilizer (Mozobil). Biochem Pharmacol. 2009;77:1655-64.
20. Arimitsu N, Shimizu J, Fujiwara N, Takai K, Takada E, Kono T, Ueda Y, Suzuki T, Suzuki N. Role of SDF1/CXCR4 interaction in experimental hemiplegic models with neural cell transplantation. Int J Mol Sci. 2012;13:2636-49.
21. Huang J, Li Y, Tang Y, Tang G, Yang G-Y, Wang Y. CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke. 2013;44:190-7.
22. Winkler EA, Sengillo JD, Sagare AP, Zhao Z, Ma Q, Zuniga E, Wang Y, Zhong Z, Sullivan JS, Griffin JH, Cleveland DW, Zlokovic BV. Blood-spinal cord barrier disruption contributes to early motor-neuron degeneration in ALS-model mice. Proc Natl Acad Sci U S A. 2014;111:E1035-42.
23. Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, O'Banion MK, Stojanovic K, Sagare A, Boillee S, Cleveland DW, Zlokovic BV. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci. 2008;11:420-2.
24. Engelhardt JI, Appel SH. IgG reactivity in the spinal cord and motor cortex in amyotrophic lateral sclerosis. Arch Neurol. 1990;47:1210-6.
25. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, Sanberg PR. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS One. 2007;2:e1205.
26. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science. 1994;264:1772-5.
27. Ezra A, Rabinovich-Nikitin I, Rabinovich-Toidman P, Solomon B. Multifunctional effect of human serum albumin reduces Alzheimer's disease related pathologies in the 3xTg mouse model. J Alzheimers Dis. 2015;50:175-88.
28. Ślusarczyk J, Trojan E, Głombik K, Budziszewska B, Kubera M, Lasoń W, Popiołek-Barczyk K, Mika J, Wȩdzony K, Basta-Kaim A. Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells. Front Cell Neurosci. 2015;9:82.
29. Fornai F, Ferrucci M, Lenzi P, Falleni A, Biagioni F, Flaibani M, Siciliano G, Giannessi F, Paparelli A. Plastic changes in the spinal cord in motor neuron disease. Biomed Res Int. 2014;2014:670756.
30. Oliván S, Calvo AC, Rando A, Muñoz MJ, Zaragoza P, Osta R. Comparative study of behavioural tests in the SOD1G93A mouse model of amyotrophic lateral sclerosis. Exp Anim. 2015;64:147-53.
31. McCombe PA, Henderson RD. The Role of immune and inflammatory mechanisms in ALS. Curr Mol Med. 2011;11:246-54.
32. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11:155-61.
33. Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol. 2007;28:299-307.
34. Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 2001;57:1282-9.
35. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res. 2009;29:313-26.
36. Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction "opening": signaling via Rho and Rho kinase. J Cell Sci. 2003;116(Pt 22):4615-28.
37. Sabelström H, Stenudd M, Frisén J. Neural stem cells in the adult spinal cord. Exp Neurol. 2014;260:44-9.
38. Hensley K, Fedynyshyn J, Ferrell S, Floyd RA, Gordon B, Grammas P, Hamdheydari L, Mhatre M, Mou S, Pye QN, Stewart C, West M, West S, Williamson KS. Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis. 2003;14:74-80.
39. Poloni M, Facchetti D, Mai R, Micheli A, Agnoletti L, Francolini G, Mora G, Camana C, Mazzini L, Bachetti T. Circulating levels of tumour necrosis factor-alpha and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci Lett. 2000;287:211-4.
40. Rossi D, Brambilla L, Valori CF, Crugnola A, Giaccone G, Capobianco R, Mangieri M, Kingston AE, Bloc A, Bezzi P, Volterra A. Defective tumor necrosis factor-alpha-dependent control of astrocyte glutamate release in a transgenic mouse model of Alzheimer disease. J Biol Chem. 2005;280:42088-96.
41. Moreau C, Devos D, Brunaud-Danel V, Defebvre L, Perez T, Destée A, Tonnel AB, Lassalle P, Just N. Elevated IL-6 and TNF-alpha levels in patients with ALS: inflammation or hypoxia? Neurology. 2005;65:1958-60.
42. Ono S, Hu J, Shimizu N, Imai T, Nakagawa H. Increased interleukin-6 of skin and serum in amyotrophic lateral sclerosis. J Neurol Sci. 2001;187:27-34.
43. Tang C-H, Chuang J-Y, Fong Y-C, Maa M-C, Way T-D, Hung C-H. Bone-derived SDF-1 stimulates IL-6 release via CXCR4, ERK and NF-kappaB pathways and promotes osteoclastogenesis in human oral cancer cells. Carcinogenesis. 2008;29:1483-92.
44. Walter HL, van der Maten G, Antunes AR, Wieloch T, Ruscher K. Treatment with AMD3100 attenuates the microglial response and improves outcome after experimental stroke. J Neuroinflammation. 2015;12:24.
45. Henkel JS, Beers DR, Wen S, Bowser R, Appel SH. Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology. 2009;72:1614-6.
46. Garbuzova-Davis S, Hernandez-Ontiveros DG, Rodrigues MCO, Haller E, Frisina-Deyo A, Mirtyl S, Sallot S, Saporta S, Borlongan CV, Sanberg PR. Impaired blood-brain/spinal cord barrier in ALS patients. Brain Res. 2012;1469:114-28.
47. Winkler EA, Sengillo JD, Sullivan JS, Henkel JS, Appel SH, Zlokovic BV. Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol. 2013;125:111-20.
48. Garbuzova-Davis S, Haller E, Saporta S, Kolomey I, Nicosia SV, Sanberg PR. Ultrastructure of blood-brain barrier and blood-spinal cord barrier in SOD1 mice modeling ALS. Brain Res. 2007;1157:126-37.
49. Johansson BB. Regeneration and plasticity in the brain and spinal cord. J Cereb Blood Flow Metab. 2007;27:1417-30.