NP001 regulation of macrophage activation markers in ALS: A phase I clinical and biomarker study

References

• McGeer PL, McGeer EG. Inflammatory processes in amyotrophic lateral sclerosis. Muscle & Nerve. 2002;26: 459–70.
   PubMed Web of Science ®Google Scholar
• Barbeito AG, Mesci P, Boillee S. Motor neuron-immune interactions: the vicious circle of ALS. J Neural Transm. 2010;117:981–1000.
   PubMed Web of Science ®Google Scholar
• McCombe PA, Henderson RD. The role of immune and inflammatory mechanisms in ALS. Current Molecular Medicine. 2011;11:246–54.
   PubMed Web of Science ®Google Scholar
• Phani S, Re DB, Przedborski S. The Role of the Innate Immune System in ALS. Frontiers in Pharmacology. 2012;3:150.
   PubMed Web of Science ®Google Scholar
• Miller RG, Mitchell JD, Lyon M, Moore DH. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev. 2007:CD001447.
   Web of Science ®Google Scholar
• Lobsiger CS, Cleveland DW. Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci. 2007;10:1355–60.
   PubMed Web of Science ®Google Scholar
• Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. CD4 + T-cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci U S A. 2008;105:15558–63.
   PubMed Web of Science ®Google Scholar
• Xiao Q, Zhao W, Beers DR, Yen AA, Xie W, Henkel JS, et al. Mutant SOD1-G93A microglia are more neurotoxic relative to wild-type microglia. Journal of Neurochemistry. 2007;102:2008–19.
   PubMed Web of Science ®Google Scholar
• Banerjee R, Mosley RL, Reynolds AD, Dhar A, Jackson-Lewis V, Gordon PH, et al. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PloS One. 2008;3:e2740.
   PubMed Web of Science ®Google Scholar
• Valente T, Mancera P, Tusell JM, Serratosa J, Saura J.C/EBPbeta expression in activated microglia in amyotrophic lateral sclerosis. Neurobiology of Aging. 2012;33:2186–99.
   PubMed Web of Science ®Google Scholar
• Akizuki M, Yamashita H, Uemura K, Maruyama H, Kawakami H, Ito H, et al. Optineurin suppression causes neuronal cell death via NF-kappaB pathway. Journal of Neurochemistry. 2013;126:699–704.
   PubMed Web of Science ®Google Scholar
• Fujita K, Izumi Y, Kaji R. Inflammatory mechanisms in amyotrophic lateral sclerosis. Brain and Nerve (Shinkei kenkyu no shinpo). 2012;64:273–8.
   PubMedGoogle Scholar
• Henkel JS, Engelhardt JI, Siklos L, Simpson EP, Kim SH, Pan T, et al. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Annals of Neurology. 2004;55:221–35.
   PubMed Web of Science ®Google Scholar
• Boillee S, Van de Velde C, Cleveland DW. ALS: a disease of motor neurons and their non-neuronal neighbors. Neuron. 2006;52:39–59.
   PubMed Web of Science ®Google Scholar
• Henkel JS, Beers DR, Zhao W, Appel SH. Microglia in ALS: the good, the bad, and the resting. J Neuroimmune Pharmacol. 2009;4:389–98.
   PubMed Web of Science ®Google Scholar
• Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. The Journal of Clinical Investigation. 2012;122: 3063–87.
   PubMed Web of Science ®Google Scholar
• Keizman D, Rogowski O, Berliner S, Ish-Shalom M, Maimon N, Nefussy B, et al. Low-grade systemic inflammation in patients with amyotrophic lateral sclerosis. Acta Neurologica Scandinavica. 2009;119:383–9.
   PubMed Web of Science ®Google Scholar
• Fiala M, Mizwicki MT, Weitzman R, Magpantay L, Nishimoto N. Tocilizumab infusion therapy normalizes inflammation in sporadic ALS patients. American Journal of Neurodegenerative Disease. 2013;2:129–39.
   PubMedGoogle Scholar
• Mizwicki MT, Fiala M, Magpantay L, Aziz N, Sayre J, Liu G, et al. Tocilizumab attenuates inflammation in ALS patients through inhibition of IL6 receptor signaling. American Journal of Neurodegenerative Disease. 2012;1: 305–15.
   PubMedGoogle Scholar
• Baron P, Bussini S, Cardin V, Corbo M, Conti G, Galimberti D, et al. Production of monocyte chemoattractant protein-1 in amyotrophic lateral sclerosis. Muscle & Nerve. 2005;32:541–4.
   PubMed Web of Science ®Google Scholar
• Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH. Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden. Neurology. 2004; 62:1758–65.
   PubMed Web of Science ®Google Scholar
• Wilms H, Sievers J, Dengler R, Bufler J, Deuschl G, Lucius R. Intrathecal synthesis of monocyte chemoattractant protein-1 (MCP-1) in amyotrophic lateral sclerosis: further evidence for microglial activation in neurodegeneration. J Neuroimmunol. 2003;144:139–42.
   PubMed Web of Science ®Google Scholar
• Zhang R, Gascon R, Miller RG, Gelinas DF, Mass J, Lancero M, et al. MCP-1 chemokine receptor CCR2 is decreased on circulating monocytes in sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2006;179:87–93.
   PubMed Web of Science ®Google Scholar
• Ono S, Hu J, Shimizu N, Imai T, Nakagawa H. Increased interleukin-6 of skin and serum in amyotrophic lateral sclerosis. Journal of the Neurological Sciences. 2001;187: 27–34.
   PubMed Web of Science ®Google Scholar
• Sekizawa T, Openshaw H, Ohbo K, Sugamura K, Itoyama Y, Niland JC. Cerebrospinal fluid interleukin 6 in amyotrophic lateral sclerosis: immunological parameter and comparison with inflammatory and non-inflammatory central nervous system diseases. Journal of the Neurological Sciences. 1998;154:194–9.
   PubMed Web of Science ®Google Scholar
• Babu GN, Kumar A, Chandra R, Puri SK, Kalita J, Misra UK. Elevated inflammatory markers in a group of amyotrophic lateral sclerosis patients from northern India. Neurochem Res. 2008;33:1145–9.
   PubMed Web of Science ®Google Scholar
• Cereda C, Baiocchi C, Bongioanni P, Cova E, Guareschi S, Metelli MR, et al. TNF and sTNFR1/2 plasma levels in ALS patients. J Neuroimmunol. 2008;194:123–31.
   PubMed Web of Science ®Google Scholar
• Poloni M, Facchetti D, Mai R, Micheli A, Agnoletti L, Francolini G, et al. Circulating levels of tumor necrosis factor-alpha and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci Lett. 2000;287:211–4.
   PubMed Web of Science ®Google Scholar
• Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurology. 2009; 8:94–109.
   PubMed Web of Science ®Google Scholar
• Zhang R, Hadlock KG, Do H, Yu S, Honrada R, Champion S, et al. Gene expression profiling in peripheral blood mononuclear cells from patients with sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2011; 230:114–23.
   PubMed Web of Science ®Google Scholar
• Zhang R, Gascon R, Miller RG, Gelinas DF, Mass J, Hadlock K, et al. Evidence for systemic immune system alterations in sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2005;159:215–24.
   PubMed Web of Science ®Google Scholar
• Zhang R, Miller RG, Gascon R, Champion S, Katz J, Lancero M, et al. Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2009;206:121–4.
   PubMed Web of Science ®Google Scholar
• Lincecum JM, Vieira FG, Wang MZ, Thompson K, de Zutter GS, Kidd J, et al. From transcriptome analysis to therapeutic anti-CD40L treatment in the SOD1 model of amyotrophic lateral sclerosis. Nat Genet. 2010;42: 392–9.
   PubMed Web of Science ®Google Scholar
• McGrath MS, Kahn JO, Herndier BG. Development of WF10, a novel macrophage-regulating agent. Curr Opin Investig Drugs. 2002;3:365–73.
   PubMedGoogle Scholar
• Joo K, Lee Y, Choi D, Han J, Hong S, Kim YM, et al. An anti-inflammatory mechanism of taurine conjugated 5-aminosalicylic acid against experimental colitis: taurine chloramine potentiates inhibitory effect of 5-aminosalicylic acid on IL-1beta-mediated NFkappaB activation. European Journal of Pharmacology. 2009;618:91–7.
   PubMed Web of Science ®Google Scholar
• Giese T, McGrath MS, Stumm S, Schempp H, Elstner E, Meuer SC. Differential effects on innate versus adaptive immune responses by WF10. Cellular Immunology. 2004;229:149–58.
   PubMed Web of Science ®Google Scholar
• McGrath MS, Miller RG, editors. Development of macrophage activation regulator NP001 for ALS. Proceedings of the 21st International Symposium on ALS/MND, Clinical Work in Progress; 2010 Dec 11–13; Orlando, USA.
   Google Scholar
• Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord.: official publication of the World Federation of Neurology, Research Group on Motor Neuron Diseases. 2000;1:293–9.
   Google Scholar
• Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). Journal of the Neurological Sciences. 1999;169:13–21.
   PubMed Web of Science ®Google Scholar
• Belge KU, Dayyani F, Horelt A, Siedlar M, Frankenberger M, Frankenberger B, et al. The proinflammatory CD14 + CD16+ DR++ monocytes are a major source of TNF. J Immunol. 2002;168:3536–42.
   PubMed Web of Science ®Google Scholar
• Scherberich JE, Nockher WA. CD14++ monocytes, CD14+/CD16 + subset and soluble CD14 as biological markers of inflammatory systemic diseases and monitoring immunosuppressive therapy. Clin Chem Lab Med. 1999; 37:209–13.
   PubMed Web of Science ®Google Scholar
• Ziegler-Heitbrock L. The CD14 + CD16+ blood monocytes: their role in infection and inflammation. Journal of Leukocyte Biology. 2007;81:584–92.
   PubMed Web of Science ®Google Scholar
• Merino A, Buendia P, Martin-Malo A, Aljama P, Ramirez R, Carracedo J. Senescent CD14 + CD16+ monocytes exhibit proinflammatory and proatherosclerotic activity. J Immunol. 2011;186:1809–15.
   PubMed Web of Science ®Google Scholar
• Sadeghi HM, Schnelle JF, Thoma JK, Nishanian P, Fahey JL. Phenotypic and functional characteristics of circulating monocytes of elderly persons. Experimental Gerontology. 1999;34:959–70.
   PubMed Web of Science ®Google Scholar
• Takeyama N, Yabuki T, Kumagai T, Takagi S, Takamoto S, Noguchi H. Selective expansion of the CD14(+)/CD16(bright) subpopulation of circulating monocytes in patients with hemophagocytic syndrome. Annals of Hematology. 2007;86:787–92.
   PubMed Web of Science ®Google Scholar
• Thieblemont N, Weiss L, Sadeghi HM, Estcourt C, Haeffner-Cavaillon N. CD14lowCD16high: a cytokine- producing monocyte subset which expands during human immunodeficiency virus infection. European Journal of Immunology. 1995;25:3418–24.
   PubMed Web of Science ®Google Scholar
• Ancuta P, Wang J, Gabuzda D. CD16 + monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1-expressing endothelial cells. Journal of Leukocyte Biology. 2006;80:1156–64.
   PubMed Web of Science ®Google Scholar
• Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L’Heureux D, Regulier EG, et al. CNS invasion by CD14+/CD16 + peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. Journal of Neurovirology. 2001;7:528–41.
   PubMed Web of Science ®Google Scholar
• Pulliam L, Gascon R, Stubblebine M, McGuire D, McGrath MS. Unique monocyte subset in patients with AIDS dementia. Lancet. 1997;349:692–5.
   PubMed Web of Science ®Google Scholar
• Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer’s disease, and multiple sclerosis. Journal of the Neurological Sciences. 2002;202: 13–23.
   PubMed Web of Science ®Google Scholar
• Ancuta P, Moses A, Gabuzda D. Transendothelial migration of CD16 + monocytes in response to fractalkine under constitutive and inflammatory conditions. Immunobiology. 2004;209:11–20.
   PubMed Web of Science ®Google Scholar
• Williams DW, Eugenin EA, Calderon TM, Berman JW. Monocyte maturation, HIV susceptibility, and transmigration across the blood-brain barrier are critical in HIV neuropathogenesis. Journal of Leukocyte Biology. 2012; 91:401–15.
   PubMed Web of Science ®Google Scholar
• Hensley K, Mhatre M, Mou S, Pye QN, Stewart C, West M, et al. On the relation of oxidative stress to neuroinflammation: lessons learned from the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Antioxidants & Redox Signaling. 2006;8:2075–87.
   PubMed Web of Science ®Google Scholar