Morphological and phagocytic profile of microglia in the developing rat cerebellum

eNeuro

Volumn 2, Issue 4, 2015, Pages

  Perez Pouchoulen, Miguel ^a   VanRyzin, Jonathan W ^a   McCarthy, Margaret M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Cell death; Development; Microglia; Phagocytosis; Sex difference; Vermis

Indexed keywords

EID: 85020795726     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0036-15.2015     Document Type: Article

References (75)

1. Abraham H, Tornóczky T, Kosztolányi G, Seress L (2001) Cell formation in the cortical layers of the developing human cerebellum. Int J Dev Neurosci 19:53–62. Medline
2. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145:399–463. CrossRef Medline
3. Altman J (1982) Morphological development of the rat cerebellum and some of its mechanism. Exp Brain Res Suppl 6:8–49.
4. Amaral DG, Schumann CM, Nordahl CW (2008) Neuroanatomy of autism. Trends Neurosci 31:137–145. CrossRef Medline
5. Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6:297–311. CrossRef Medline
6. Apps R, Hawkes R (2009) Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10:670–681. CrossRef Medline
7. Ashwell K (1990) Microglia and cell death in the developing mouse cerebellum. Dev Brain Res 55:219–230. Medline
8. Auger AP, Olesen KM (2009) Brain sex differences and the organisation of juvenile social play behaviour. J Neuroendocrinol 21: 519–525. CrossRef Medline
9. Ayoub AE, Salm AK (2003) Increased morphological diversity of microglia in the activated hypothalamic supraoptic nucleus. J Neurosci 23:7759–7766. Medline
10. Bauman ML, Kemper TL (2005) Neuroanatomic observations of the brain in autism: a review and future directions. Int J Dev Neurosci 23:183–187. CrossRef Medline
11. Berbel P, Innocenti GM (1988) The development of the corpus callosum in cats: a light- and electron-microscopic study. J Comp Neurol 276:132–156. CrossRef Medline
12. Burgoyne RD, Cambray-Deakin MA (1988) The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res 472:77–101. Medline
13. Butts T, Green MJ, Wingate RJ (2014) Development of the cerebellum: simple steps to make a “little brain”. Development 141:4031– 4041. CrossRef Medline
14. Carletti B, Rossi F (2008) Neurogenesis in the cerebellum. Neuroscientist 14:91–100. CrossRef Medline
15. Cǎtǎlin B, Cupido A, Iancǎu M, Albu CV, Kirchhoff F (2013) Microglia: first responders in the central nervous system. Rom J Morphol Embryol 54:467–472. Medline
16. Cuadros MA, Rodríguez-Ruiz J, Calvente R, Almendros A, Marín- Teva JL, Navascués J (1997) Microglia development in the quail cerebellum. J Comp Neurol 389:390–401. Medline
17. D’Amelio M, Sheng M, Cecconi F (2012) Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci 35:700–709.
18. Dean SL, McCarthy MM (2008) Steroids, sex and the cerebellar cortex: implications for human disease. Cerebellum 7:38–47. CrossRef Medline
19. Durisko C, Fiez JA (2010) Functional activation in the cerebellum during working memory and simple speech tasks. Cortex 46:896– 906. CrossRef Medline
20. Friauf E (1992) Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur J Neurosci 4:798–812. Medline
21. Glickstein M (1992) The cerebellum and motor learning. Curr Opin Neurobiol 2:802–806. Medline
22. Glickstein M, Strata P, Voogd J (2009) Cerebellum: history. Neuroscience 162:549–559. CrossRef Medline
23. Goldowitz D, Hamre K (1998) The cells and molecules that make a cerebellum. Trends Neurosci 21:375–382. Medline
24. Gómez-Gonzalez B, Escobar A (2010) Prenatal stress alters microglial development and distribution in postnatal rat brain. Acta Neuropathol 119:303–315. CrossRef Medline
25. Gottwald B, Mihajlovic Z, Wilde B, Mehdorn HM (2003) Does the cerebellum contribute to specific aspects of attention? Neuropsychologia 41:1452–1460. Medline
26. Haraguchi S, Sasahara K, Shikimi H, Honda S, Harada N, Tsutsui K (2012) Estradiol promotes purkinje dendritic growth, spinogenesis, and synaptogenesis during neonatal life by inducing the expression of BDNF. Cerebellum 11:416–417. CrossRef Medline
27. Hashimoto K, Kano M (2005) Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci Res 53:221–228. CrossRef Medline
28. Heinsen H (1977) Quantitative anatomical studies on the postnatal development of the cerebellum of the albino rat. Anat Embryol (Berl) 151:201–218. Medline
29. Holstege G, Georgiadis JR, Paans AM, Meiners LC, van der Graaf FH, Reinders AA (2003) Brain activation during human male ejaculation. J Neurosci 23:9185–9193. Medline
30. Hyman BT, Yuan J (2012) Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci 13:395–406. CrossRef Medline
31. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1–9. Medline
32. Kaur C, Sivakumar V, Zou Z, Ling EA (2014) Microglia-derived proinflammatory cytokines tumor necrosis factor-alpha and interleukin-1beta induce Purkinje neuronal apoptosis via their receptors in hypoxic neonatal rat brain. Brain Struct Funct 219:151– 170. CrossRef Medline
33. Lenz KM, Nugent BM, Haliyur R, McCarthy MM (2013) Microglia are essential to masculinization of brain and behavior. J Neurosci 33:2761–2772. CrossRef Medline
34. Lossi L, Mioletti S, Merighi A (2002) Synapse-independent and synapse-dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages. Neuroscience 112:509–523. Medline
35. Marín-Teva JL, Dusart I, Colin C, Gervais A, van Rooijen N, Mallat M (2004) Microglia promote the death of developing Purkinje cells. Neuron 41:535–547. Medline
36. McKay BE, Turner RW (2005) Physiological and morphological development of the rat cerebellar Purkinje cell. J Physiol 567:829– 850. CrossRef Medline
37. Meaney M, Stewart J (1981) A descriptive study of social development in the rat (rattus norvegicus). Anim Behav 29:34–45. Cross-Ref
38. Miquel M, Toledo R, García LI, Coria-Avila GA, Manzo J (2009) Why should we keep the cerebellum in mind when thinking about addiction? Curr Drug Abuse Rev 2:26–40. Medline
39. Moulton EA, Elman I, Becerra LR, Goldstein RZ, Borsook D (2014) The cerebellum and addiction: insights gained from neuroimaging research. Addict Biol 19:317–331. Medline
40. Moulton EA, Schmahmann JD, Becerra L, Borsook D (2010) The cerebellum and pain: passive integrator or active participator? Brain Res Rev 65:14–27. CrossRef Medline
41. Murdoch BE (2010) The cerebellum and language: historical perspective and review. Cortex 46:858–868. CrossRef Medline
42. Nayak D, Roth TL, McGavern DB (2014) Microglia development and function. Annu Rev Immunol 32:367–402. CrossRef Medline
43. Neumann H, Kotter MR, Franklin RJ (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132:288–295. CrossRef Medline
44. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314–1318. CrossRef Medline
45. Oomman S, Finckbone V, Dertien J, Attridge J, Henne W, Medina M, Mansouri B, Singh H, Strahlendorf H, Strahlendorf J (2004) Active caspase-3 expression during postnatal development of rat cerebellum is not systematically or consistently associated with apoptosis. J Comp Neurol 476:154–173. CrossRef Medline
46. Panksepp J (1981) The ontogeny of play in rats. Dev Psychobiol 14:327–332. CrossRef Medline
47. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456–1458. CrossRef Medline
48. Parnaik R, Raff MC, Scholes J (2000) Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr Biol 10:857–860. Medline
49. Perez-Pouchoulen M, Miquel M, Saft P, Brug B, Toledo R, Hernandez ME, Manzo J (2012) The cerebellum in Autism. e-Neurobiologia 3:1–11.
50. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119–145. CrossRef Medline
51. Rapoport M, van Reekum R, Mayberg H (2000) The role of the cerebellum in cognition and behavior: a selective review. J Neu-ropsychiatry Clin Neurosci 12:193–198. Medline
52. Reiter LW, Anderson GE, Laskey JW, Cahill DF (1975) Developmental and behavioral changes in the rat during chronic exposure to lead. Environ Health Perspect 12:119–123. Medline
53. Saab CY, Willis WD (2003) The cerebellum: organization, functions and its role in nociception. Brain Res Brain Res Rev 42:85–95. Medline
54. Sarna JR, Hawkes R (2003) Patterned Purkinje cell death in the cerebellum. Prog Neurobiol 70:473–507. Medline
55. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691–705. CrossRef Medline
56. Schwarz JM, Sholar PW, Bilbo SD (2012) Sex differences in microglial colonization of the developing rat brain. J Neurochem 120: 948–963. CrossRef Medline
57. Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22:526–539. CrossRef Medline
58. Sierra A, Abiega O, Shahraz A, Neumann H (2013) Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6. CrossRef Medline
59. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495. CrossRef Medline
60. Sillitoe RV, Joyner AL (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23:549–577. CrossRef Medline
61. Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295–339. CrossRef Medline
62. Strata P (2015) The emotional cerebellum. Cerebellum. Advance online publication. doi:10.1007/s12311-015-0649-9.
63. Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434. CrossRef Medline
64. Swanson JA (2008) Shaping cups into phagosomes and macropi-nosomes. Nat Rev Mol Cell Biol 9:639–649. CrossRef Medline
65. Tanaka M (2009) Dendrite formation of cerebellar Purkinje cells. Neurochem Res 34:2078–2088. CrossRef Medline
66. ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen HO, Renier WO (2003) Development and developmental disorders of the human cerebellum. J Neurol 250:1025–1036. CrossRef Medline
67. Tremblay ME, Lowery RL, Majewska AK (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8:e1000527. CrossRef Medline
68. Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A (2011) The role of microglia in the healthy brain. J Neurosci 31: 16064–16069. CrossRef Medline
69. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57:67–81. CrossRef Medline
70. Vela JM, Dalmau I, González B, Castellano B (1995) Morphology and distribution of microglial cells in the young and adult mouse cerebellum. J Comp Neurol 361:602–616. CrossRef Medline
71. Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21:370–375. Medline
72. Werling DM, Geschwind DH (2013) Sex differences in autism spectrum disorders. Curr Opin Neurol 26:146–153. CrossRef Medline
73. Williamson LL, Sholar PW, Mistry RS, Smith SH, Bilbo SD (2011) Microglia and memory: modulation by early-life infection. J Neurosci 31:15511–15521. CrossRef Medline
74. Wood KA, Dipasquale B, Youle RJ (1993) In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11:621– 632. Medline
75. Wu CH, Wen CY, Shieh JY, Ling EA (1992) A quantitative and morphometric study of the transformation of amoeboid microglia into ramified microglia in the developing corpus callosum in rats. J Anat 181:423–430.