Skip to main content
SpringerLink
Log in

Microglia-Müller Cell Interactions in the Retina

  • Conference paper
  • First Online:
Book cover Retinal Degenerative Diseases

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 801))

Abstract

Microglia and Müller cells are cell types that feature prominently in responses to disease and injury in the retina. However, their mutual interactions have not been investigated in detail. Here, we review evidence that indicate that these two cell populations exchange functionally significant signals under uninjured conditions and during retinal inflammation. Under normal conditions, Müller cells constitute a potential source of extracellular ATP that mediates the activity-dependent regulation of microglial dynamic process motility. Following microglial activation in inflammation, microglia can signal to Müller cells, influencing their morphological, molecular, and functional responses. Microglia-Müller cell interactions appear to be a mode of bi-directional communications that help shape the overall injury response in the retina.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Wake H, Moorhouse AJ, Nabekura J (2011) Functions of microglia in the central nervous system-beyond the immune response. Neuron Glia Biol 7(1):47–53

    Article  PubMed  Google Scholar 

  2. Ransohoff RM, Cardona AE (2011) The myeloid cells of the central nervous system parenchyma. Nature 468(7321):253–262

    Article  CAS  Google Scholar 

  3. Buffo A, Rolando C, Ceruti S (2010) Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential. Biochem Pharmacol 79(2):77–89

    Article  PubMed  CAS  Google Scholar 

  4. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387–1394

    Article  PubMed  CAS  Google Scholar 

  5. Santos AM, Calvente R, Tassi M, Carrasco MC, Martin-Oliva D, Marin-Teva JL et al (2008) Embryonic and postnatal development of microglial cells in the mouse retina. J Comp Neurol 506(2):224–239

    Article  PubMed  Google Scholar 

  6. Karlstetter M, Ebert S, Langmann T (2010) Microglia in the healthy and degenerating retina: insights from novel mouse models. Immunobiology 215(9–10):685–691

    Article  PubMed  CAS  Google Scholar 

  7. Bringmann A, Iandiev I, Pannicke T, Wurm A, Hollborn M, Wiedemann P et al (2009) Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 28(6):423–451

    Article  PubMed  CAS  Google Scholar 

  8. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN et al (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25(4):397–424

    Article  PubMed  CAS  Google Scholar 

  9. Newman EA, Zahs KR (1998) Modulation of neuronal activity by glial cells in the retina. J Neurosci 18(11):4022–4028

    PubMed Central  PubMed  CAS  Google Scholar 

  10. Poitry-Yamate CL, Poitry S, Tsacopoulos M (1995) Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J Neurosci 15(7 Pt 2):5179–5191

    PubMed  CAS  Google Scholar 

  11. Bringmann A, Wiedemann P (2012) Muller glial cells in retinal disease. Ophthalmologica 227(1):1–19

    Article  PubMed  Google Scholar 

  12. Xu H, Chen M, Forrester JV (2009) Para-inflammation in the aging retina. Prog Retin Eye Res 28(5):348–368

    Article  PubMed  CAS  Google Scholar 

  13. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S et al (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8(6):752–758

    Article  PubMed  CAS  Google Scholar 

  14. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318

    Article  PubMed  CAS  Google Scholar 

  15. Fontainhas AM, Wang M, Liang KJ, Chen S, Mettu P, Damani M et al (2011) Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 6(1):e15973

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Lee JE, Liang KJ, Fariss RN, Wong WT (2008) Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest Ophthalmol Vis Sci 49(9):4169–4176

    Article  PubMed Central  PubMed  Google Scholar 

  17. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN et al (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 50(9):4444–4451

    Article  PubMed Central  PubMed  Google Scholar 

  18. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119–145

    Article  PubMed  CAS  Google Scholar 

  19. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19(8):312–318

    Article  PubMed  CAS  Google Scholar 

  20. Trapp BD, Wujek JR, Criste GA, Jalabi W, Yin X, Kidd GJ et al (2007) Evidence for synaptic stripping by cortical microglia. Glia 55(4):360–368

    Article  PubMed  Google Scholar 

  21. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29(13):3974–3980

    Article  PubMed  CAS  Google Scholar 

  22. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP 2nd et al (2006) Microglia instruct subventricular zone neurogenesis. Glia 54(8):815–825

    Article  PubMed  Google Scholar 

  23. Elkabes S, DiCicco-Bloom EM, Black IB (1996) Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16(8):2508–2521

    PubMed  CAS  Google Scholar 

  24. Harada T, Harada C, Kohsaka S, Wada E, Yoshida K, Ohno S et al (2002) Microglia-Muller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci 22(21):9228–9236

    PubMed  CAS  Google Scholar 

  25. Bessis A, Bechade C, Bernard D, Roumier A (2007) Microglial control of neuronal death and synaptic properties. Glia 55(3):233–238

    Article  PubMed  Google Scholar 

  26. Roumier A, Pascual O, Bechade C, Wakselman S, Poncer JC, Real E et al (2008) Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS One 3(7):e2595

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R et al (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691–705

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  28. Li Y, Du XF, Liu CS, Wen ZL, Du JL (2012) Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev Cell 23(6):1189–1202

    Article  PubMed  CAS  Google Scholar 

  29. Uckermann O, Wolf A, Kutzera F, Kalisch F, Beck-Sickinger AG, Wiedemann P et al (2006) Glutamate release by neurons evokes a purinergic inhibitory mechanism of osmotic glial cell swelling in the rat retina: activation by neuropeptide Y. J Neurosci Res 83(4):538–550

    Article  PubMed  CAS  Google Scholar 

  30. Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. Pflugers Arch 452(5):589–597

    Article  PubMed  CAS  Google Scholar 

  31. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277(12):10482–10488

    Article  PubMed  CAS  Google Scholar 

  32. Dahl G, Locovei S (2006) Pannexin: to gap or not to gap, is that a question? IUBMB Life 58(7):409–419

    Article  PubMed  CAS  Google Scholar 

  33. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E (2009) Pannexin 1: the molecular substrate of astrocyte “hemichannels”. J Neurosci 29(21):7092–7097

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  34. Balasingam V, Dickson K, Brade A, Yong VW (1996) Astrocyte reactivity in neonatal mice: apparent dependence on the presence of reactive microglia/macrophages. Glia 18(1):11–26

    Article  PubMed  CAS  Google Scholar 

  35. Graeber MB, Kreutzberg GW (1988) Delayed astrocyte reaction following facial nerve axotomy. J Neurocytol 17(2):209–220

    Article  PubMed  CAS  Google Scholar 

  36. Sawada M, Suzumura A, Marunouchi T (1995) Cytokine network in the central nervous system and its roles in growth and differentiation of glial and neuronal cells. Int J Dev Neurosci 13(3–4):253–264

    Article  PubMed  CAS  Google Scholar 

  37. Wang M, Ma W, Zhao L, Fariss RN, Wong WT (2011) Adaptive Muller cell responses to microglial activation mediate neuroprotection and coordinate inflammation in the retina. J Neuroinflammation 8:173

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unit on Neuron-Glia Interactions in Retinal Diseases, National Eye Institute, National Institutes of Health, 6 Center Drive, 6/215, 20892, Bethesda, MD, USA

    Minhua Wang & Wai T. Wong

Authors
  1. Minhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wai T. Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wai T. Wong .

Editor information

Editors and Affiliations

  1. Department of Ophthalmology, University of Florida, Gainesville, Florida, USA

    John D. Ash

  2. University Hospital Zurich, Zurich, Switzerland

    Christian Grimm

  3. Cole Eye Institute at the Cleveland Clin Division of Ophthalmology, Cleveland, Ohio, USA

    Joe G. Hollyfield

  4. Dean A. McGee Eye Inst., University of Oklahoma Health Science Center, Oklahoma City, Oklahoma, USA

    Robert E. Anderson

  5. Beckman Vision Center, University of California, San Francisco School of Medicine, San Francisco, California, USA

    Matthew M. LaVail

  6. Department of Ophthalmology, Duke University Medical Center, Durham, North Carolina, USA

    Catherine Bowes Rickman

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media, LLC

About this paper

Cite this paper

Wang, M., Wong, W. (2014). Microglia-Müller Cell Interactions in the Retina. In: Ash, J., Grimm, C., Hollyfield, J., Anderson, R., LaVail, M., Bowes Rickman, C. (eds) Retinal Degenerative Diseases. Advances in Experimental Medicine and Biology, vol 801. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3209-8_42

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-3209-8_42

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4614-3208-1

  • Online ISBN: 978-1-4614-3209-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation