A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS

Journal of Neuroscience

Volumn 30, Issue 25, 2010, Pages 8676-8691

  Tabor Godwin, Jenna M ^a   Ruller, Chelsea M ^a   Bagalso, Nolan ^a   An, Naili ^b   Pagarigan, Robb R ^b,c   Harkins, Stephanie ^b   Gilbert, Paul E ^a   Kiosses, William B ^b   Gude, Natalie A ^a   Cornell, Christopher T ^b,d   Doran, Kelly S ^a   Sussman, Mark A ^a   Whitton, J Lindsay ^b   Feuer, Ralph ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d ALLERGAN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BONE MARROW CELL; BRAIN INFECTION; CELL ISOLATION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CHOROID PLEXUS; COXSACKIE VIRUS INFECTION; IMMUNOFLUORESCENCE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANIMALS, NEWBORN; CHOROID PLEXUS; COXSACKIEVIRUS INFECTIONS; FLUORESCENT ANTIBODY TECHNIQUE; IN SITU HYBRIDIZATION; MICE; MICROSCOPY, CONFOCAL; MYELOID CELLS; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 77954124160     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1860-10.2010     Document Type: Article

References (51)

1. Alvarez-Buylla A, Seri B, Doetsch F (2002) Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57:751-758. (Pubitemid 34522150)
2. Berger JR, Chumley W, Pittman T, Given C, Nuovo G (2006) Persistent coxsackie B encephalitis: report of a case and review of the literature. J Neurovirol 12:511-516.
3. Brazelton TR, Rossi FM, Keshet GI, Blau HM (2000) From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775-1779. (Pubitemid 32004810)
4. Campbell GR, Spector SA (2008) CCL2 increases X4-tropic HIV-1 entry into resting CD4+ T cells. J Biol Chem 283:30745-30753.
5. Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
6. Castro RF, Jackson KA, Goodell MA, Robertson CS, Liu H, Shine HD (2002) Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297:1299. (Pubitemid 34913161)
7. Chen N, Hudson JE, Walczak P, Misiuta I, Garbuzova-Davis S, Jiang L, Sanchez-Ramos J, Sanberg PR, Zigova T, Willing AE (2005) Human umbilical cord blood progenitors: the potential of these hematopoietic cells to become neural. Stem Cells 23:1560-1570. (Pubitemid 41741005)
8. Courtioux B, Boda C, Vatunga G, Pervieux L, Josenando T, M'Eyi PM, Bouteille B, Jauberteau-Marchan MO, Bisser S (2006) A link between chemokine levels and disease severity in human African trypanosomiasis. Int J Parasitol 36:1057-1065. (Pubitemid 44107934)
9. Dar A, Kollet O, Lapidot T (2006) Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp Hematol 34:967-975. (Pubitemid 44080383)
10. Dickson PW, Aldred AR, Marley PD, Bannister D, Schreiber G (1986) Rat choroid plexus specializes in the synthesis and the secretion of transthyretin (prealbumin). Regulation of transthyretin synthesis in choroid plexus is independent from that in liver. J Biol Chem 261:3475-3478.
11. Doetsch F, Caille I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716. (Pubitemid 29278045)
12. Emerich DF, Skinner SJ, Borlongan CV, Vasconcellos AV, Thanos CG (2005) The choroid plexus in the rise, fall and repair of the brain. Bioessays 27:262-274. (Pubitemid 40476489)
13. Esfandiarei M, Luo H, Yanagawa B, Suarez A, Dabiri D, Zhang J, McManus BM (2004) Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J Virol 78:4289-4298. (Pubitemid 38437232)
14. Eugenin EA, Osiecki K, Lopez L, Goldstein H, Calderon TM, Berman JW (2006) CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: a potential mechanism of HIV-CNS invasion and neuroAIDS. J Neurosci 26:1098-1106. (Pubitemid 43237041)
15. Falk A, Frisén J (2002) Amphiregulin is a mitogen for adult neural stem cells. J Neurosci Res 69:757-762. (Pubitemid 34984693)
16. Feuer R, Whitton JL (2008) Preferential coxsackievirus replication in proliferating/activated cells: implications for virus tropism, persistence, and pathogenesis. Curr Top Microbiol Immunol 323:149-173.
17. Feuer R, Mena I, Pagarigan R, Slifka MK, Whitton JL (2002) Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol 76:4430-4440. (Pubitemid 34309580)
18. Feuer R, Mena I, Pagarigan RR, Harkins S, Hassett DE, Whitton JL (2003) Coxsackievirus B3 and the neonatal CNS: the roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am J Pathol 163:1379-1393. (Pubitemid 37175086)
19. Feuer R, Mena I, Pagarigan RR, Hassett DE, Whitton JL (2004) Coxsackievirus replication and the cell cycle: a potential regulatory mechanism for viral persistence/latency. Med Microbiol Immunol 193:83-90. (Pubitemid 38703775)
20. Feuer R, Pagarigan RR, Harkins S, Liu F, Hunziker IP, Whitton JL (2005) Coxsackievirus targets proliferating neuronal progenitor cells in the neonatal CNS. J Neurosci 25:2434-2444. (Pubitemid 40322286)
21. Feuer R, Ruller CM, An N, Tabor-Godwin JM, Rhoades RE, Maciejewski S, Pagarigan RR, Cornell CT, Crocker SJ, Kiosses WB, Pham-Mitchell N, Campbell IL, Whitton JL (2009) Viral persistence and chronic immunopathology in the adult central nervous system following coxsackievirus infection during the neonatal period. J Virol 83:9356-9369.
22. Helfand BT, Chang L, Goldman RD (2003) The dynamic and motile properties of intermediate filaments. Annu Rev Cell Dev Biol 19:445-467. (Pubitemid 37487356)
23. Ho MK, Springer TA (1983) Tissue distribution, structural characterization, and biosynthesis of Mac-3, a macrophage surface glycoprotein exhibiting molecular weight heterogeneity. J Biol Chem 258:636-642.
24. Ito D, Tanaka K, Suzuki S, Dembo T, Fukuuchi Y (2001) Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32:1208-1215. (Pubitemid 32825812)
25. Itokazu Y, Kitada M, Dezawa M, Mizoguchi A, Matsumoto N, Shimizu A, Ide C (2006) Choroid plexus ependymal cells host neural progenitor cells in the rat. Glia 53:32-42. (Pubitemid 43076210)
26. Kleeberger W, Bova GS, Nielsen ME, Herawi M, Chuang AY, Epstein JI, Berman DM (2007) Roles for the stem cell associated intermediate filament Nestin in prostate cancer migration and metastasis. Cancer Res 67:9199-9206. (Pubitemid 47535906)
27. Kodama H, Inoue T, Watanabe R, Yasuoka H, Kawakami Y, Ogawa S, Ikeda Y, Mikoshiba K, Kuwana M (2005) Cardiomyogenic potential of mesenchymal progenitors derived from human circulating CD14+ monocytes. Stem Cells Dev 14:676-686.
28. Kodama H, Inoue T, Watanabe R, Yasutomi D, Kawakami Y, Ogawa S, Mikoshiba K, Ikeda Y, Kuwana M (2006) Neurogenic potential of progenitors derived from human circulating CD14+ monocytes. Immunol Cell Biol 84:209-217.
29. Kramer M, Schulte BM, Toonen LW, Barral PM, Fisher PB, Lanke KH, Galama JM, van Kuppeveld FJ, Adema GJ (2008) Phagocytosis of picornavirus-infected cells induces an RNA-dependent antiviral state in human dendritic cells. J Virol 82:2930-2937.
30. Krizhanovsky V, Ben-Arie N (2006) A novel role for the choroid plexus in BMP-mediated inhibition of differentiation of cerebellar neural progenitors. Mech Dev 123:67-75.
31. Kuwana M, Okazaki Y, Kodama H, Izumi K, Yasuoka H, Ogawa Y, Kawakami Y, Ikeda Y (2003) Human circulating CD14+ monocytes as a source of progenitors that exhibit mesenchymal cell differentiation. J Leukoc Biol 74:833-845.
32. Lawrence S, Tang Y, Frank MB, Dozmorov I, Jiang K, Chen Y, Cadwell C, Turner S, Centola M, Jarvis JN (2007) A dynamic model of gene expression in monocytes reveals differences in immediate/early response genes between adult and neonatal cells. J Inflamm (Lond) 4:4.
33. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
34. Massengale M, Wagers AJ, Vogel H, Weissman IL (2005) Hematopoietic cells maintain hematopoietic fates upon entering the brain. J Exp Med 201:1579-1589.
35. Mercier F, Kitasako JT, Hatton GI (2002) Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol 451:170-188. (Pubitemid 34920408)
36. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR (2000) Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290:1779-1782. (Pubitemid 32004811)
37. Nagai M, Yaoita E, Yoshida Y, Kuwano R, Nameta M, Ohshiro K, Isome M, Fujinaka H, Suzuki S, Suzuki J, Suzuki H, Yamamoto T (2003) Coxsackievirus and adenovirus receptor, a tight junction membrane protein, is expressed in glomerular podocytes in the kidney. Lab Invest 83:901-911. (Pubitemid 36723699)
38. Nataf S, Strazielle N, Hatterer E, Mouchiroud G, Belin MF, Ghersi-Egea JF (2006) Rat choroid plexuses contain myeloid progenitors capable of differentiation toward macrophage or dendritic cell phenotypes. Glia 54:160-171. (Pubitemid 44230853)
39. Nervi B, Link DC, DiPersio JF (2006) Cytokines and hematopoietic stem cell mobilization. J Cell Biochem 99:690-705. (Pubitemid 44521989)
40. Noda S, Aguirre SA, Bitmansour A, Brown JM, Sparer TE, Huang J, Mocarski ES (2006) Cytomegalovirus MCK-2 controls mobilization and recruitment of myeloid progenitor cells to facilitate dissemination. Blood 107:30-38. (Pubitemid 43053519)
41. Ransohoff RM, Kivisäkk P, Kidd G (2003) Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3:569-581. (Pubitemid 37328676)
42. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F (2009) C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 10:514-523.
43. Refojo D, Echenique C, Müller MB, Reul JM, Deussing JM, Wurst W, Sillaber I, Paez-Pereda M, Holsboer F, Arzt E (2005) Corticotropin-releasing hormone activates ERK1/2 MAPK in specific brain areas. Proc Natl Acad Sci U S A 102:6183-6188.
44. Romero JR (2008) Pediatric group B coxsackievirus infections. Curr Top Microbiol Immunol 323:223-239.
45. Saitoh A, Sawyer MH, Leake JA (2004) Acute disseminated encephalomyelitis associated with enteroviral infection. Pediatr Infect Dis J 23:1174-1175.
46. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-120.
47. Strunk T, Temming P, Gembruch U, Reiss I, Bucsky P, Schultz C (2004) Differential maturation of the innate immune response in human fetuses. Pediatr Res 56:219-226.
48. Takeuchi O, Akira S (2009) Innate immunity to virus infection. Immunol Rev 227:75-86.
49. Verboon-Maciolek MA, Groenendaal F, Cowan F, Govaert P, van Loon AM, de Vries LS (2006) White matter damage in neonatal enterovirus meningoencephalitis. Neurology 66:1267-1269.
50. Vitry S, Bertrand JY, Cumano A, Dubois-Dalcq M (2003) Primordial hematopoietic stem cells generate microglia but not myelin-forming cells in a neural environment. J Neurosci 23:10724-10731.
51. Whitton JL, Cornell CT, Feuer R (2005) Host and virus determinants of picornavirus pathogenesis and tropism. Nat Rev Microbiol 3:765-776.