Differential regulation of macrophage phenotype by mature and pro-nerve growth factor

Journal of Neuroimmunology

Volumn 285, Issue , 2015, Pages 76-93

  Williams, Kimberly S ^a,b   Killebrew, Deirdre A ^a   Clary, Gillian P ^a   Seawell, Jaimie A ^a   Meeker, Rick B ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Actin; Calcium; Inflammation; Monocyte; Neurodegeneration; Neurotrophin

Indexed keywords

GROWTH FACTOR; NERVE GROWTH FACTOR; NEUROTOXIN; NEUROTROPHIN RECEPTOR; NEUROTROPHIN RECEPTOR P75; PRO NERVE GROWTH FACTOR; PROTEIN PRECURSOR; PROTEIN TYROSINE KINASE A; UNCLASSIFIED DRUG; PRO-NERVE GROWTH FACTOR, HUMAN;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL MIGRATION; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PODOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; REGULATORY MECHANISM; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; DRUG EFFECTS; FEMALE; LONG EVANS RAT; MONONUCLEAR CELL; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; NERVE GROWTH FACTOR; PHENOTYPE; PROTEIN PRECURSORS; RATS; RATS, LONG-EVANS;

EID: 84943264900     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2015.05.016     Document Type: Article

References (58)

1. Al-Shawi R., Hafner A., Chun S., Raza S., Crutcher K., Thrasivoulou C., Simons P., Cowen T. ProNGF, sortilin, and age-related neurodegeneration. Ann. N. Y. Acad. Sci. 2007, 1119:208-215.
2. Aronica E., Ozbas-Gerceker F., Redeker S., Ramkema M., Spliet W.G., Van Rijen P.C., Leenstra S., Gorter J.A., Troost D. Expression and cellular distribution of high- and low-affinity neurotrophin receptors in malformations of cortical development. Acta Neuropathol. 2004, 108:422-434.
3. Artico M., Bronzetti E., Felici L.M., Alicino V., Ionta B., Bronzetti B., Magliulo G., Grande C., Zamai L., Pasquantonio G., De Vincentiis M. Neurotrophins and their receptors in human lingual tonsil: an immunohistochemical analysis. Oncol. Rep. 2008, 20:1201-1206.
4. Barouch R., Appel E., Kazimirsky G., Brodie C. Macrophages express neurotrophins and neurotrophin receptors. Regulation of nitric oxide production by NT-3. J. Neuroimmunol. 2001, 112:72-77.
5. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8:57-69.
6. Bragg D.C., Hudson L.C., Liang Y.H., Tompkins M.B., Fernandes A., Meeker R.B. Choroid plexus macrophages proliferate and release toxic factors in response to feline immunodeficiency virus. J. Neurovirol. 2002, 8:225-239.
7. Buccione R., Orth J.D., Mcniven M.A. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 2004, 5:647-657.
8. Capsoni S., Brandi R., Arisi I., D'Onofrio M., Cattaneo A. A dual mechanism linking NGF/proNGF imbalance and early inflammation to Alzheimer's disease neurodegeneration in the AD11 anti-NGF mouse model. CNS Neurol. Disord. Drug Targets 2011, 10:635-647.
9. Carvalho B., Clark D.J., Angst M.S. Local and systemic release of cytokines, nerve growth factor, prostaglandin E2, and substance P in incisional wounds and serum following cesarean delivery. J. Pain 2008, 9:650-657.
10. Curtis M.M., Way S.S. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 2009, 126:177-185.
11. Dowling P., Ming X., Raval S., Husar W., Casaccia-Bonnefil P., Chao M., Cook S., Blumberg B. Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology 1999, 53:1676-1682.
12. Elkabes S., Peng L., Black I.B. Lipopolysaccharide differentially regulates microglial trk receptor and neurotrophin expression. J. Neurosci. Res. 1998, 54:117-122.
13. Garaci E., Caroleo M.C., Aloe L., Aquaro S., Piacentini M., Costa N., Amendola A., Micera A., Calio R., Perno C.F., Levi-Montalcini R. Nerve growth factor is an autocrine factor essential for the survival of macrophages infected with HIV. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:14013-14018.
14. Giulian D., Vaca K., Noonan C.A. Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 1990, 250:1593-1596.
15. Giulian D., Yu J., Li X., Tom D., Li J., Wendt E., Lin S.N., Schwarcz R., Noonan C. Study of receptor-mediated neurotoxins released by HIV-1-infected mononuclear phagocytes found in human brain. J. Neurosci. 1996, 16:3139-3153.
16. Harrington A.W., Leiner B., Blechschmitt C., Arevalo J.C., Lee R., Morl K., Meyer M., Hempstead B.L., Yoon S.O., Giehl K.M. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6226-6230.
17. Hempstead B.L. Commentary: regulating proNGF action: multiple targets for therapeutic intervention. Neurotox. Res. 2009, 16:255-260.
18. Hikawa S., Kobayashi H., Hikawa N., Kusakabe T., Hiruma H., Takenaka T., Tomita T., Kawakami T. Expression of neurotrophins and their receptors in peripheral lung cells of mice. Histochem. Cell Biol. 2002, 118:51-58.
19. Hoffmann A., Kann O., Ohlemeyer C., Hanisch U.K., Kettenmann H. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J. Neurosci. 2003, 23:4410-4419.
20. Huang Da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
21. Huang Da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
22. Ibanez C.F. Jekyll-Hyde neurotrophins: the story of proNGF. Trends Neurosci. 2002, 25:284-286.
23. Kruskal B.A., Maxfield F.R. Cytosolic free calcium increases before and oscillates during frustrated phagocytosis in macrophages. J. Cell Biol. 1987, 105:2685-2693.
24. Krygier S., Djakiew D. Neurotrophin receptor p75 (NTR) suppresses growth and nerve growth factor-mediated metastasis of human prostate cancer cells. Int. J. Cancer 2002, 98:1-7.
25. Laskin D.L., Sunil V.R., Gardner C.R., Laskin J.D. Macrophages and tissue injury: agents of defense or destruction?. Annu. Rev. Pharmacol. Toxicol. 2011, 51:267-288.
26. Le A.P., Friedman W.J. Matrix metalloproteinase-7 regulates cleavage of pro-nerve growth factor and is neuroprotective following kainic acid-induced seizures. J. Neurosci. 2012, 32:703-712.
27. Levanti M.B., Germana A., Catania S., Germana G.P., Gauna-Anasco L., Vega J.A., Ciriaco E. Neurotrophin receptor-like proteins in the bovine (Bos taurus) lymphoid organs, with special reference to thymus and spleen. Anat. Histol. Embryol. 2001, 30:193-198.
28. Levi-Montalcini R., Skaper S.D., Dal Toso R., Petrelli L., Leon A. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci. 1996, 19:514-520.
29. Malemud C.J. Matrix metalloproteinases (MMPs) in health and disease: an overview. Front. Biosci. 2006, 11:1696-1701.
30. Martin S., Vincent J.P., Mazella J. Involvement of the neurotensin receptor-3 in the neurotensin-induced migration of human microglia. J. Neurosci. 2003, 23:1198-1205.
31. Martin S., Dicou E., Vincent J.P., Mazella J. Neurotensin and the neurotensin receptor-3 in microglial cells. J. Neurosci. Res. 2005, 81:322-326.
32. Meeker R.B., Poulton W., Feng W.H., Hudson L., Longo F.M. Suppression of immunodeficiency virus-associated neural damage by the p75 neurotrophin receptor ligand, LM11A-31, in an in vitro feline model. J. Neuroimmune Pharmacol. 2012, 7:388-400.
33. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11:723-737.
34. Myers J.T., Swanson J.A. Calcium spikes in activated macrophages during Fcgamma receptor-mediated phagocytosis. J. Leukoc. Biol. 2002, 72:677-684.
35. Nakajima K., Kikuchi Y., Ikoma E., Honda S., Ishikawa M., Liu Y., Kohsaka S. Neurotrophins regulate the function of cultured microglia. Glia 1998, 24:272-289.
36. Nico B., Mangieri D., Benagiano V., Crivellato E., Ribatti D. Nerve growth factor as an angiogenic factor. Microvasc. Res. 2008, 75:135-141.
37. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., Jacobsen C., Kliemannel M., Schwarz E., Willnow T.E., Hempstead B.L., Petersen C.M. Sortilin is essential for proNGF-induced neuronal cell death. Nature 2004, 427:843-848.
38. O'Donnell L.A., Agrawal A., Jordan-Sciutto K.L., Dichter M.A., Lynch D.R., Kolson D.L. Human immunodeficiency virus (HIV)-induced neurotoxicity: roles for the NMDA receptor subtypes. J. Neurosci. 2006, 26:981-990.
39. Ohsawa K., Imai Y., Kanazawa H., Sasaki Y., Kohsaka S. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J. Cell Sci. 2000, 113(Pt 17):3073-3084.
40. Patel P.C., Harrison R.E. Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 2008, 19:4628-4639.
41. Pulliam L., Herndier B., Tang N., Mcgrath M. Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J. Clin. Investig. 1991, 87:506-512.
42. Pulliam L., Clarke J.A., Mcgrath M.S., Moore D., Mcguire D. Monokine products as predictors of AIDS dementia. AIDS 1996, 10:1495-1500.
43. RansohoffR.M., Perry V.H. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 2009, 27:119-145.
44. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1545-1564.
45. Samah B., Porcheray F., Gras G. Neurotrophins modulate monocyte chemotaxis without affecting macrophage function. Clin. Exp. Immunol. 2008, 151:476-486.
46. Samah B., Porcheray F., Dereuddre-Bosquet N., Gras G. Nerve growth factor stimulation promotes CXCL-12 attraction of monocytes but decreases human immunodeficiency virus replication in attracted population. J. Neurovirol. 2009, 15:71-80.
47. Szklarczyk A., Conant K., Owens D.F., Ravin R., McKay R.D., Gerfen C. Matrix metalloproteinase-7 modulates synaptic vesicle recycling and induces atrophy of neuronal synapses. Neuroscience 2007, 149:87-98.
48. Tiveron C., Fasulo L., Capsoni S., Malerba F., Marinelli S., Paoletti F., Piccinin S., Scardigli R., Amato G., Brandi R., Capelli P., D'Aguanno S., Florenzano F., La Regina F., Lecci A., Manca A., Meli G., Pistillo L., Berretta N., Nistico R., Pavone F., Cattaneo A. ProNGF\NGF imbalance triggers learning and memory deficits, neurodegeneration and spontaneous epileptic-like discharges in transgenic mice. Cell Death Differ. 2013, 20:1017-1030.
49. Tonchev A.B., Boneva N.B., Kaplamadzhiev D.B., Kikuchi M., Mori Y., Sahara S., Yamashima T. Expression of neurotrophin receptors by proliferating glia in postischemic hippocampal CA1 sector of adult monkeys. J. Neuroimmunol. 2008, 205:20-24.
50. Tovar-y-Romo L.B., Kolson D.L., Bandaru V.V., Drewes J.L., Graham D.R., Haughey N.J. Adenosine triphosphate released from HIV-infected macrophages regulates glutamatergic tone and dendritic spine density on neurons. J. Neuroimmune Pharmacol. 2013, 8:998-1009.
51. Urshansky N., Mausner-Fainberg K., Auriel E., Regev K., Farhum F., Karni A. Dysregulated neurotrophin mRNA production by immune cells of patients with relapsing remitting multiple sclerosis. J. Neurol. Sci. 2010, 295:31-37.
52. Vaegter C.B., Jansen P., Fjorback A.W., Glerup S., Skeldal S., Kjolby M., Richner M., Erdmann B., Nyengaard J.R., Tessarollo L., Lewin G.R., Willnow T.E., Chao M.V., Nykjaer A. Sortilin associates with Trk receptors to enhance anterograde transport and neurotrophin signaling. Nat. Neurosci. 2011, 14:54-61.
53. White M.G., Wang Y., Akay C., Lindl K.A., Kolson D.L., Jordan-Sciutto K.L. Parallel high throughput neuronal toxicity assays demonstrate uncoupling between loss of mitochondrial membrane potential and neuronal damage in a model of HIV-induced neurodegeneration. Neurosci. Res. 2011, 70:220-229.
54. Wong I., Liao H., Bai X., Zaknic A., Zhong J., Guan Y., Li H.Y., Wang Y.J., Zhou X.F. ProBDNF inhibits infiltration of ED1+ macrophages after spinal cord injury. Brain Behav. Immun. 2010, 24:585-597.
55. Xia J., Wang F., Wang L., Fan Q. Elevated serine protease HtrA1 inhibits cell proliferation, reduces invasion, and induces apoptosis in esophageal squamous cell carcinoma by blocking the nuclear factor-kappaB signaling pathway. Tumour Biol. 2013, 34:317-328.
56. Xiong H., Zeng Y.C., Lewis T., Zheng J., Persidsky Y., Gendelman H.E. HIV-1 infected mononuclear phagocyte secretory products affect neuronal physiology leading to cellular demise: relevance for HIV-1-associated dementia. J. Neurovirol. 2000, 6(Suppl. 1):S14-S23.
57. Zhang X., Angkasekwinai P., Dong C., Tang H. Structure and function of interleukin-17 family cytokines. Protein Cell 2011, 2:26-40.
58. Zhu S., Qian Y. IL-17/IL-17 receptor system in autoimmune disease: mechanisms and therapeutic potential. Clin. Sci. 2012, 122:487-511.