CoChat
Sign Up
Cited by 145Virus-based gene therapy researchNeuroinflammation and Neurodegeneration MechanismsRNA Interference and Gene Delivery

Targeting microglia with lentivirus and AAV: Recent advances and remaining challenges

Open access
Maes, Margaret E., Colombo, Gloria, Schulz, Rouven, Siegert, Sandra·2019·Neuroscience Letters
DOI 10.1016/j.neulet.2019.134310PMC PMC6734419
Open this paper in CoChat — free accountOpen PDF

Abstract

Microglia have emerged as a critical component of neurodegenerative diseases. Genetic manipulation of microglia can elucidate their functional impact in disease. In neuroscience, recombinant viruses such as lentiviruses and adeno-associated viruses (AAVs) have been successfully used to target various cell types in the brain, although effective transduction of microglia is rare. In this review, we provide a short background of lentiviruses and AAVs, and strategies for designing recombinant viral vectors. Then, we will summarize recent literature on successful microglial transductions in vitro and in vivo, and discuss the current challenges. Finally, we provide guidelines for reporting the efficiency and specificity of viral targeting in microglia, which will enable the microglial research community to assess and improve methodologies for future studies.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neulet.2019.134310

Cites

21 of 21 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Alterations in microglia can lead to alterations in behavior in mice.

    “It is widely known that alterations in microglia can lead to alterations in behavior in mice5,13–15.”

    From Constitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia (2026) · cites this paper as [13]

  • The CX3CR1 receptor is involved in neuron-microglia fractalkine signaling, which plays a vital role in microglial developmental synaptic pruning and homeostasis.

    “The CX3CR1 receptor is involved in neuron-microglia fractalkine signaling, which plays a vital role in microglial developmental synaptic pruning and homeostasis.”

    From Constitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia (2026) · cites this paper as [13]

    The Microglia-specific transgene expression section describes a Cx3cr1-based mouse model for targeting microglia, but does not discuss the receptor’s signaling function. Searches for fractalkine signaling and developmental synaptic pruning found no passage in our copy linking CX3CR1 to those processes or to homeostasis; the nearby references do not establish that claim. (LLM, conf=0.73)

    Experimental — accuracy not yet measured

  • Loss and deficiency of the CX3CR1 receptor can alter microglial number, subsequently altering microglia-mediated synaptic pruning during developmental ages.

    “Its loss and deficiency can alter microglial number, subsequently altering microglia-mediated synaptic pruning during developmental ages13,18.”

    From Constitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia (2026) · cites this paper as [13]

    The Microglia-specific transgene expression section (page unavailable) discusses a Cx3cr1-based mouse model as a way to target microglia, not the effects of losing the receptor. Searches for CX3CR1 deficiency, microglial number, and developmental synaptic pruning found no passage in our copy addressing the claimed sequence of effects. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 82

  1. [1]Salter M.W. Stevens B. Microglia emerge as central players in brain disease Nat. Med. 23 2017 1018 1027 28886007
  2. [2]Kim Y.S. Joh T.H. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson’s disease Exp. Mol. Med. 38 2006 333 347 16953112
  3. [3]Rajendran L. Paolicelli R.C. Microglia-mediated synapse loss in alzheimer’s disease J. Neurosci. 38 2018 2911 2919 29563239 PMC6596066
  4. [4]Parr-Brownlie L.C. Bosch-Bouju C. Schoderboeck L. Sizemore R.J. Abraham W.C. Hughes S.M. Lentiviral vectors as tools to understand central nervous system biology in mammalian model organisms Front. Mol. Neurosci. 8 2015 14 26041987 PMC4434958
  5. [5]Enquist L.W. Card J.P. Recent advances in the use of neurotropic viruses for circuit analysis Curr. Opin. Neurobiol. 13 2003 603 606 14630225
  6. [6]Vannucci L. Lai M. Chiuppesi F. Ceccherini-Nelli L. Pistello M. Viral vectors: a look back and ahead on gene transfer technology New Microbiol. 36 2013 1 22 23435812
  7. [8]Lewis P.F. Emerman M. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus J. Virol. 68 1994 510 516 http://www.ncbi.nlm.nih.gov/pubmed/8254763 8254763 PMC236313
  8. [9]Lewis P. Hensel M. Emerman M. Human immunodeficiency virus infection of cells arrested in the cell cycle EMBO J. 11 1992 3053 3058 http://www.ncbi.nlm.nih.gov/pubmed/1322294 1322294 PMC556788
  9. [11]Zufferey R. Nagy D. Mandel R.J. Naldini L. Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo Nat. Biotechnol. 15 1997 871 875 9306402
  10. [12]Yu S.F. von Rüden T. Kantoff P.W. Garber C. Seiberg M. Rüther U. Anderson W.F. Wagner E.F. Gilboa E. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells Proc. Natl. Acad. Sci. U. S. A. 83 1986 3194 3198 http://www.ncbi.nlm.nih.gov/pubmed/3458176 3458176 PMC323479
  11. [13]Zufferey R. Dull T. Mandel R.J. Bukovsky A. Quiroz D. Naldini L. Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery J. Virol. 1998 99030895 PMC110499 9811723
  12. [14]Miyoshi H. Blömer U. Takahashi M. Gage F.H. Verma I.M. Development of a self-inactivating lentivirus vector J. Virol. 72 1998 8150 8157 http://www.ncbi.nlm.nih.gov/pubmed/9733856 9733856 PMC110156
  13. [15]Dull T. Zufferey R. Kelly M. Mandel R.J. Nguyen M. Trono D. Naldini L. A third-generation lentivirus vector with a conditional packaging system J. Virol. 1998 98440501 PMC110254 9765382
  14. [16]Cronin J. Zhang X.-Y. Reiser J. Altering the tropism of lentiviral vectors through pseudotyping Curr. Gene Ther. 5 2005 387 398 16101513 PMC1368960
  15. [17]Finkelshtein D. Werman A. Novick D. Barak S. Rubinstein M. LDL receptor and its family members serve as the cellular receptors for vesicular stomatitis virus Proc. Natl. Acad. Sci. 110 2013 7306 7311 23589850 PMC3645523
  16. [18]Burns J.C. Friedmann T. Driever W. Burrascano M. Yee J.K. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells Proc. Natl. Acad. Sci. 1993 PMC47282 8396259
  17. [19]Su W. Kang J. Sopher B. Gillespie J. Aloi M.S. Odom G.L. Hopkins S. Case A. Wang D.B. Chamberlain J.S. Garden G.A. Recombinant adeno-associated viral (rAAV) vectors mediate efficient gene transduction in cultured neonatal and adult microglia J. Neurochem. 136 2016 49 62 25708596 PMC4547919
  18. [20]Balcaitis S. Weinstein J.R. Li S. Chamberlain J.S. Möller T. Lentiviral transduction of microglial cells Glia 50 2005 48 55 15625717
  19. [21]Jiang X. Ni Y. Liu T. Zhang M. Ren H. Jiang R. Huang X. Xu G. CCR2 overexpression promotes the efficient recruitment of retinal microglia in vitro Mol. Vis. 18 2012 2982 2992 http://www.ncbi.nlm.nih.gov/pubmed/23288990 23288990 PMC3534147
  20. [22]Masuda T. Tsuda M. Tozaki-Saitoh H. Inoue K. Lentiviral transduction of cultured microglia Methods Mol. Biol. 1041 2013 63 67 23813370
  21. [23]Åkerblom M. Sachdeva R. Quintino L. Wettergren E.E. Chapman K.Z. Manfre G. Lindvall O. Lundberg C. Jakobsson J. Visualization and genetic modification of resident brain microglia using lentiviral vectors regulated by microRNA-9 Nat. Commun. 4 2013 23612311
  22. [24]Brawek B. Liang Y. Savitska D. Li K. Fomin-Thunemann N. Kovalchuk Y. Zirdum E. Jakobsson J. Garaschuk O. A new approach for ratiometric in vivo calcium imaging of microglia Sci. Rep. 7 2017 1 13 28729628 PMC5519759
  23. [25]Nie X. Kitaoka S. Tanaka K. Segi-Nishida E. Imoto Y. Ogawa A. Nakano F. Tomohiro A. Nakayama K. Taniguchi M. Mimori-Kiyosue Y. Kakizuka A. Narumiya S. Furuyashiki T. The innate immune receptors TLR2/4 mediate repeated social defeat stress-induced social avoidance through prefrontal microglial activation Neuron 99 2018 464 479 e7 30033154
  24. [26]Parkhurst C.N. Yang G. Ninan I. Savas J.N. Yates J.R. Lafaille J.J. Hempstead B.L. Littman D.R. Gan W.-B. Gan W.-B. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor Cell. 155 2013 1596 1609 24360280 PMC4033691
  25. [28]Cukor G. Blacklow N.R. Hoggan M.D. Berns K.I. Biology of adeno-associated virus The Parvoviruses 1984 Springer Berlin, Heidelberg 33 66
  26. [29]Berns K.I. Parvovirus replication Microbiol. Rev. 54 1990 316 329 http://www.ncbi.nlm.nih.gov/pubmed/2215424 2215424 PMC372780
  27. [30]Atchison R.W. Casto B.C. Hammon W.M. Adenovirus-associated defective virus particles Science (80-.) 149 1965 754 755 14325163
  28. [31]Schnepp B.C. Jensen R.L. Chen C.-L. Johnson P.R. Clark K.R. Characterization of adeno-associated virus genomes isolated from human tissues J. Virol. 79 2005 14793 14803 16282479 PMC1287572
  29. [32]Große S. Penaud-Budloo M. Herrmann A.-K. Börner K. Fakhiri J. Laketa V. Krämer C. Wiedtke E. Gunkel M. Ménard L. Ayuso E. Grimm D. Relevance of assembly-activating protein for Adeno-associated virus vector production and capsid protein stability in mammalian and insect cells J. Virol. 91 2017 JVI.01198-17 PMC5625497 28768875
  30. [33]Weitzman M.D. Linden R.M. Adeno-associated virus biology Methods Mol. Biol. 807 2011 1 23 22034024
  31. [34]Linden R.M. Ward P. Giraud C. Winocour E. Berns K.I. Site-specific integration by adeno-associated virus Proc. Natl. Acad. Sci. 93 1996 11288 11294 8876128 PMC38050
  32. [35]Wu Z. Asokan A. Samulski R.J. Adeno-associated virus serotypes: vector toolkit for human gene therapy Mol. Ther. 14 2006 316 327 16824801
  33. [36]Bedbrook C.N. Deverman B.E. Gradinaru V. Viral strategies for targeting the central and peripheral nervous systems Annu. Rev. Neurosci. 41 2018 323 348 29709207
  34. [39]Aschauer D.F. Kreuz S. Rumpel S. Analysis of Transduction Efficiency, Tropism and Axonal Transport of AAV Serotypes 1, 2, 5, 6, 8 and 9 in the Mouse Brain PLoS One 8 2013 e76310 PMC3785459 24086725
  35. [40]Hammond S.L. Leek A.N. Richman E.H. Tjalkens R.B. Cellular selectivity of AAV serotypes for gene delivery in neurons and astrocytes by neonatal intracerebroventricular injection PLoS One 12 2017 e0188830 PMC5731760 29244806
  36. [41]Petrosyan H.A. Alessi V. Singh V. Hunanyan A.S. Levine J.M. Arvanian V.L. Transduction efficiency of neurons and glial cells by AAV-1, -5, -9, -rh10 and -hu11 serotypes in rat spinal cord following contusion injury Gene Ther. 21 2014 991 1000 25119378
  37. [42]Zincarelli C. Soltys S. Rengo G. Rabinowitz J.E. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection Mol. Ther. 16 2008 1073 1080 18414476
  38. [43]Burger C. Gorbatyuk O.S. Velardo M.J. Peden C.S. Williams P. Zolotukhin S. Reier P.J. Mandel R.J. Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system Mol. Ther. 10 2004 302 317 15294177
  39. [44]Kanaan N.M. Sellnow R.C. Boye S.L. Coberly B. Bennett A. Agbandje-McKenna M. Sortwell C.E. Hauswirth W.W. Boye S.E. Manfredsson F.P. Rationally engineered AAV capsids improve transduction and volumetric spread in the CNS Mol. Ther. - Nucleic Acids. 8 2017 184 197 28918020 PMC5503098
  40. [45]Choudhury S.R. Harris A.F. Cabral D.J. Keeler A.M. Sapp E. Ferreira J.S. Gray-Edwards H.L. Johnson J.A. Johnson A.K. Su Q. Stoica L. DiFiglia M. Aronin N. Martin D.R. Gao G. Sena-Esteves M. Widespread central nervous system gene transfer and silencing after systemic delivery of novel AAV-AS vector Mol. Ther. 24 2016 726 735 26708003 PMC4886933
  41. [46]Cearley C.N. Wolfe J.H. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain Mol. Ther. 13 2006 528 537 16413228
  42. [47]McCarty D.M. Self-complementary AAV vectors; advances and applications Mol. Ther. 16 2008 1648 1656 18682697
  43. [48]Wu J. Zhao W. Zhong L. Han Z. Li B. Ma W. Weigel-Kelley K.A. Warrington K.H. Srivastava A. Self-complementary recombinant adeno-associated viral vectors: packaging capacity and the role of rep proteins in vector purity Hum. Gene Ther. 18 2007 171 182 17328683
  44. [49]Bartlett J.S. Samulski R.J. McCown T.J. Selective and rapid uptake of adeno-associated virus type 2 in brain Hum. Gene Ther. 9 1998 1181 1186 9625257
  45. [50]Cucchiarini M. Ren X.L. Perides G. Terwilliger E.F. Selective gene expression in brain microglia mediated via adeno-associated virus type 2 and type 5 vectors Gene Ther. 10 2003 657 667 12692594
  46. [51]Rosario A.M. Cruz P.E. Ceballos-Diaz C. Strickland M.R. Siemienski Z. Pardo M. Schob K.-L. Li A. Aslanidi G.V. Srivastava A. Golde T.E. Chakrabarty P. Microglia-specific targeting by novel capsid-modified AAV6 vectors Mol. Ther. - Methods Clin. Dev. 3 2016 16026 27308302 PMC4909093
  47. [52]Pandya J. Ortiz L. Ling C. Rivers A.E. Aslanidi G. Rationally designed capsid and transgene cassette of AAV6 vectors for dendritic cell-based cancer immunotherapy Immunol. Cell Biol. 92 2014 116 123 24217810
  48. [53]Aslanidi G.V. Rivers A.E. Ortiz L. Govindasamy L. Ling C. Jayandharan G.R. Zolotukhin S. Agbandje-McKenna M. Srivastava A. High-efficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors Vaccine 30 2012 3908 3917 22497875 PMC3356484
  49. [54]Ussher J.E. Taylor J.A. Optimized transduction of human monocyte-derived dendritic cells by recombinant adeno-associated virus serotype 6 Hum. Gene Ther. 21 2010 1675 1686 20578847
  50. [55]Zhong L. Li B. Mah C.S. Govindasamy L. Agbandje-McKenna M. Cooper M. Herzog R.W. Zolotukhin I. Warrington K.H. Weigel-Van Aken K.A. Hobbs J.A. Zolotukhin S. Muzyczka N. Srivastava A. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses Proc. Natl. Acad. Sci. U. S. A. 105 2008 7827 7832 18511559 PMC2402387
  51. [56]Grace P.M. Wang X. Strand K.A. Baratta M.V. Zhang Y. Galer E.L. Yin H. Maier S.F. Watkins L.R. DREADDed microglia in pain: implications for spinal inflammatory signaling in male rats Exp. Neurol. 304 2018 125 131 29530713 PMC5916033
  52. [57]Grace P.M. Strand K.A. Galer E.L. Urban D.J. Wang X. Baratta M.V. Fabisiak T.J. Anderson N.D. Cheng K. Greene L.I. Berkelhammer D. Zhang Y. Ellis A.L. Yin H.H. Campeau S. Rice K.C. Roth B.L. Maier S.F. Watkins L.R. Morphine paradoxically prolongs neuropathic pain in rats by amplifying spinal NLRP3 inflammasome activation Proc. Natl. Acad. Sci. 113 2016 E3441 E3450 27247388 PMC4914184
  53. [58]Deverman B.E. Pravdo P.L. Simpson B.P. Kumar S.R. Chan K.Y. Banerjee A. Wu W.L. Yang B. Huber N. Pasca S.P. Gradinaru V. Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain Nat. Biotechnol. 34 2016 204 209 26829320 PMC5088052
  54. [60]Chakrabarty P. Rosario A. Cruz P. Siemienski Z. Ceballos-Diaz C. Crosby K. Jansen K. Borchelt D.R. Kim J.Y. Jankowsky J.L. Golde T.E. Levites Y. Capsid serotype and timing of injection determines AAV transduction in the neonatal mice brain PLoS One 8 2013 e67680 PMC3692458 23825679
  55. [62]Kaul M. Garden G.A. Lipton S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia Nature. 410 2001 988 994 11309629
  56. [63]Doms R.W. Trono D. The plasma membrane as a combat zone in the HIV battlefield Genes Dev. 14 2000 2677 2688 11069884
  57. [64]Heng T.S.P. Painter M.W. Elpek K. Lukacs-Kornek V. Mauermann N. Turley S.J. Koller D. Kim F.S. Wagers A.J. Asinovski N. Davis S. Fassett M. Feuerer M. Gray D.H.D. Haxhinasto S. Hill J.A. Hyatt G. Laplace C. Leatherbee K. Mathis D. Benoist C. Jianu R. Laidlaw D.H. Best J.A. Knell J. Goldrath A.W. Jarjoura J. Sun J.C. Zhu Y. Lanier L.L. Ergun A. Li Z. Collins J.J. Shinton S.A. Hardy R.R. Friedline R. Sylvia K. Kang J. The Immunological Genome Project: networks of gene expression in immune cells Nat. Immunol. 9 2008 1091 1094 18800157
  58. [65]Siegert S. Cabuy E. Scherf B.G. Kohler H. Panda S. Le Y.Z. Fehling H.J. Gaidatzis D. Stadler M.B. Roska B. Transcriptional code and disease map for adult retinal cell types Nat. Neurosci. 15 2012 487 495 22267162
  59. [66]Summerford C. Bartlett J.S. Samulski R.J. αVβ5 integrin: a co-receptor for adeno-associated virus type 2 infection Nat. Med. 5 1999 78 82 9883843
  60. [70]Qing K. Mah C. Hansen J. Zhou S. Dwarki V. Srivastava A. Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2 Nat. Med. 5 1999 71 77 9883842
  61. [71]Wu Z. Miller E. Agbandje-McKenna M. Samulski R.J. Kozyreva O.G. Samulski R.J. Parent K.N. Baker T.S. Agbandje-McKenna M. 2,3 and 2,6 N-Linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6 J. Virol. 80 2006 9093 9103 16940521 PMC1563919
  62. [72]Ng R. Govindasamy L. Gurda B.L. McKenna R. Kozyreva O.G. Samulski R.J. Parent K.N. Baker T.S. Agbandje-McKenna M. Structural characterization of the dual glycan binding adeno-associated virus serotype 6 J. Virol. 84 2010 12945 12957 20861247 PMC3004313
  63. [73]Huang L.-Y. Patel A. Ng R. Miller E.B. Halder S. McKenna R. Asokan A. Agbandje-McKenna M. Characterization of the adeno-associated virus 1 and 6 sialic acid binding site J. Virol. 90 2016 5219 5230 26962225 PMC4934739
  64. [74]Huang L.Y. Halder S. Agbandje-Mckenna M. Parvovirus glycan interactions Curr. Opin. Virol. 7 2014 108 118 25047752 PMC4149944
  65. [76]Sullivan J.A. Stanek L.M. Lukason M.J. Bu J. Osmond S.R. Barry E.A. O’Riordan C.R. Shihabuddin L.S. Cheng S.H. Scaria A. Rationally designed AAV2 and AAVrh8R capsids provide improved transduction in the retina and brain Gene Ther. 25 2018 205 219 29785047
  66. [77]Mercer J. Greber U.F. Virus interactions with endocytic pathways in macrophages and dendritic cells Trends Microbiol. 21 2013 380 388 23830563
  67. [78]Borsotti C. Borroni E. Follenzi A. Lentiviral vector interactions with the host cell Curr. Opin. Virol. 21 2016 102 108 27637073
  68. [79]Kettenmann H. Hanisch U.-K. Noda M. Verkhratsky A. Physiology of microglia Physiol. Rev. 91 2011 461 553 21527731
  69. [80]Wes P.D. Holtman I.R. Boddeke E.W.G.M. Möller T. Eggen B.J.L. Next generation transcriptomics and genomics elucidate biological complexity of microglia in health and disease Glia 64 2016 197 213 26040959
  70. [83]Belur L.R. Temme A. Podetz-Pedersen K.M. Riedl M. Vulchanova L. Robinson N. Hanson L.R. Kozarsky K.F. Orchard P.J. Frey W.H. Low W.C. McIvor R.S. Intranasal adeno-associated virus mediated gene delivery and expression of human iduronidase in the central nervous system: a noninvasive and effective approach for prevention of neurologic disease in mucopolysaccharidosis type I Hum. Gene Ther. 28 2017 576 587 28462595 PMC5549804
  71. [84]Simon V. Bloch N. Landau N.R. Intrinsic host restrictions to HIV-1 and mechanisms of viral escape Nat. Immunol. 16 2015 546 553 25988886 PMC6908429
  72. [85]Doyle T. Goujon C. Malim M.H. HIV-1 and interferons: Who’s interfering with whom? Nat. Rev. Microbiol. 13 2015 403 413 25915633 PMC7768976
  73. [87]Berry G.E. Asokan A. Cellular transduction mechanisms of adeno-associated viral vectors Curr. Opin. Virol. 21 2016 54 60 27544821 PMC5138113
  74. [88]Wang J. Faust S.M. Rabinowitz J.E. The next step in gene delivery: molecular engineering of adeno-associated virus serotypes J. Mol. Cell. Cardiol. 50 2011 793 802 21029739
  75. [89]Schultz B.R. Chamberlain J.S. Recombinant adeno-associated virus transduction and integration Mol. Ther. 16 2008 1189 1199 18500252 PMC2574934
  76. [90]Kelich J.M. Ma J. Dong B. Wang Q. Chin M. Magura C.M. Xiao W. Yang W. Super-resolution imaging of nuclear import of adeno-associated virus in live cells Mol. Ther. - Methods Clin. Dev. 2 2015 15047 26665132 PMC4667716
  77. [91]Leuci V. Mesiano G. Gammaitoni L. Cammarata C. Capellero S. Todorovic M. Jordaney N. Circosta P. Elia A. Lesnikova M. Georges G.E. Piacibello W. Fagioli F. Cignetti A. Aglietta M. Sangiolo D. Transient proteasome inhibition as a strategy to enhance lentiviral transduction of hematopoietic CD34 + cells and T lymphocytes: implications for the use of low viral doses and large-size vectors J. Biotechnol. 156 2011 218 226 21933686
  78. [94]Rabinowitz S.S. Gordon S. Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli J. Exp. Med. 174 1991 827 836 1919437 PMC2118958
  79. [97]Thion M.S. Low D. Silvin A. Chen J. Grisel P. Schulte-Schrepping J. Blecher R. Ulas T. Squarzoni P. Hoeffel G. Coulpier F. Siopi E. David F.S. Scholz C. Shihui F. Lum J. Amoyo A.A. Larbi A. Poidinger M. Buttgereit A. Lledo P.M. Greter M. Chan J.K.Y. Amit I. Beyer M. Schultze J.L. Schlitzer A. Pettersson S. Ginhoux F. Garel S. Microbiome influences prenatal and adult microglia in a sex-specific manner Cell. 172 2018 500 516 e16 29275859 PMC5786503
  80. [99]Saunders A. Sabatini B.L. Cre activated and inactivated recombinant adeno-associated viral vectors for neuronal anatomical tracing or activity manipulation Curr. Protoc. Neurosci. 2015 2015 1.24.1-1.24.15 PMC4545963 26131660
  81. [102]Parkhurst C.N. Yang G. Ninan I. Savas J.N. Yates J.R. Lafaille J.J. Hempstead B.L. Littman D.R. Gan W.B. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor Cell. 155 2013 1596 1609 24360280 PMC4033691
  82. [103]Saunders A. Johnson C.A. Sabatini B.L. Novel recombinant adeno-associated viruses for Cre activated and inactivated transgene expression in neurons Front. Neural Circuits 6 2012 PMC3406316 22866029

Cited by

Sorted by citations

Authors
Maes, M. E., Colombo, G., Schulz, R., & Siegert, S.
Affiliations
Institute of Science and Technology Austria (AT)
Corresponding author
Siegert, Sandra
ORCID
Venue
Neuroscience Letters
Publisher
Elsevier BV
Published
2019-08
Volume
707
Pages
134310
ISSN
0304-3940 (ISSN-L)
DOI
10.1016/j.neulet.2019.134310
PMC
PMC6734419
OpenAlex
W2947020292
Cited by
145
References
21
Citations by year
2026: 14 · 2025: 22 · 2024: 33 · 2023: 18 · 2022: 23 · 2021: 19 · 2020: 16
FWCI
1.92
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuroscience Letters (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • H2020 Marie Skłodowska-Curie Actions
  • European Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
Keywords
microglia, lentivirus, adeno-associated virus, viral vector design, neurodegenerative diseases
MeSH terms
Dependovirus, Animals, Genetic Vectors, Humans, Transduction, Genetic, HIV-1, Lentivirus, Microglia, Gene Targeting

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review