期刊论文详细信息
Fluids and Barriers of the CNS
Visualisation of cerebrospinal fluid flow patterns in albino Xenopus larvae in vivo
Ryuji Toyoizumi1  Susumu Izumi1  Takeshi Adachi1  Kazue Mogi1 
[1] Department of Biological Science, Kanagawa University, Tsuchiya 2946, Hiratsuka city 259-1293, Japan
关键词: Polystyrene beads;    Qdot nanocrystals;    Visualisation;    Albino larva;    Xenopus laevis;    Brain ventricle;    Left-right asymmetry;    Dorso-ventral asymmetry;    CSF flow;   
Others  :  807291
DOI  :  10.1186/2045-8118-9-9
 received in 2011-12-27, accepted in 2012-04-25,  发布年份 2012
PDF
【 摘 要 】

Background

It has long been known that cerebrospinal fluid (CSF), its composition and flow, play an important part in normal brain development, and ependymal cell ciliary beating as a possible driver of CSF flow has previously been studied in mammalian fetuses in vitro. Lower vertebrate animals are potential models for analysis of CSF flow during development because they are oviparous. Albino Xenopus laevis larvae are nearly transparent and have a straight, translucent brain that facilitates the observation of fluid flow within the ventricles. The aim of these experiments was to study CSF flow and circulation in vivo in the developing brain of living embryos, larvae and tadpoles of Xenopus laevis using a microinjection technique.

Methods

The development of Xenopus larval brain ventricles and the patterns of CSF flow were visualised after injection of quantum dot nanocrystals and polystyrene beads (3.1 or 5.8 μm in diameter) into the fourth cerebral ventricle at embryonic/larval stages 30-53.

Results

The fluorescent nanocrystals showed the normal development of the cerebral ventricles from embryonic/larval stages 38 to 53. The polystyrene beads injected into stage 47-49 larvae revealed three CSF flow patterns, left-handed, right-handed and non-biased, in movement of the beads into the third ventricle from the cerebral aqueduct (aqueduct of Sylvius). In the lateral ventricles, anterior to the third ventricle, CSF flow moved anteriorly along the outer wall of the ventricle to the inner wall and then posteriorly, creating a semicircle. In the cerebral aqueduct, connecting the third and fourth cerebral ventricles, CSF flow moved rostrally in the dorsal region and caudally in the ventral region. Also in the fourth ventricle, clear dorso-ventral differences in fluid flow pattern were observed.

Conclusions

This is the first visualisation of the orchestrated CSF flow pattern in developing vertebrates using a live animal imaging approach. CSF flow in Xenopus albino larvae showed a largely consistent pattern, with the exception of individual differences in left-right asymmetrical flow in the third ventricle.

【 授权许可】

   
2012 Mogi et al; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140708104917168.pdf 6341KB PDF download
Figure 5. 131KB Image download
Figure 4. 113KB Image download
Figure 3. 261KB Image download
Figure 2. 115KB Image download
Figure 1. 116KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Taketomo T, Saito A: Experimental studies on cerebrospinal fluid flow. Neurology 1965, 15:578-586.
  • [2]Enzmann DR, Pelc NJ: Cerebrospinal fluid flow measured by phase-contrast cine MR. Am J Neuroradiol 1993, 14:1301-1307. discussion 1309-1310
  • [3]Bradley WG Jr, Scalzo D, Queralt J, Nitz WN, Atkinson DJ, Wong P: Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 1996, 198:523-529.
  • [4]Greitz D, Hannerz J: A proposed model of cerebrospinal fluid circulation: observations with radionuclide cisternography. Am J Neuroradiol 1996, 17:431-438.
  • [5]Nelson DJ, Wright EM: The distribution, activity, and function of the cilia in the frog brain. J Physiol 1974, 243:63-78.
  • [6]Bradley WG Jr, Kortman KE, Burgoyne B: Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images. Radiology 1986, 159:611-616.
  • [7]Greitz D, Hannerz J, Rähn T, Bolander H, Ericsson A: MR imaging of cerebrospinal fluid dynamics in health and disease. On the vascular pathogenesis of communicating hydrocephalus and benign intracranial hypertension. Acta Radiol 1994, 35:204-211.
  • [8]Blackshear PJ, Graves JP, Stumpo DJ, Cobos I, Rubenstein JL, Zeldin DC: Graded phenotypic response to partial and complete deficiency of a brain-specific transcript variant of the winged helix transcription factor RFX4. Development 2003, 130:4539-4552.
  • [9]Chiang WW, Takoudis CG, Lee SH, Weis-Mcnulty A, Glick R, Alperin N: Relationship between ventricular morphology and aqueductal cerebrospinal fluid flow in healthy and communicating hydrocephalus. Invest Radiol 2009, 44:192-199.
  • [10]Jones HC: Fenestration of the epithelium lining the roof of the fourth cerebral ventricle in amphibia. Cell Tissue Res 1979, 198:129-136.
  • [11]Jones HC, Jopling CA: The development of interependymal pores in the rhombencephalic posterior tela in late embryonic, larval and metamorphosing stages of Rana pipiens. Brain Res 1983, 283:121-130.
  • [12]Jones HC: Continuity between the ventricular and subarachnoid cerebrospinal fluid in an amphibian, Rana pipiens. Cell Tissue Res 1978, 195:153-167.
  • [13]Jones HC: Circulation of marker substances in the cerebrospinal fluid of an amphibian, Rana pipiens. Cell Tissue Res 1980, 211:317-330.
  • [14]Jones HC, Dack S, Ellis C: Morphological aspects of the development of hydrocephalus in a mouse mutant (SUMS/NP). Acta Neuropathol 1987, 72:268-276.
  • [15]Mirzadeh Z, Han YG, Soriano-Navarro M, García-Verdugo JM, Alvarez-Buylla A: Cilia organize ependymal planar polarity. J Neurosci 2010, 30:2600-2610.
  • [16]Kishimoto N, Sawamoto K: Planar polarity of ependymal cilia. Differentiation 2012, 83:S86-90.
  • [17]Nieuwkoop PD, Faber J: External and internal stage criteria in the development of Xenopus laevis. In Normal table of Xenopus laevis. Amsterdam: Elsevier/North Holland Co; 1967:162-188.
  • [18]Bruchez M Jr, Moronne M, Gin P, Weiss S, Alivisatos AP: Semiconductor nanocrystals as fluorescent biological labels. Science 1998, 281:2013-2016.
  • [19]Hoshino A, Fujioka K, Oku T, Nakamura S, Suga M, Yamaguchi Y, Suzuki K, Yasuhara M, Yamamoto K: Quantum dots targeted to the assigned organelle in living cells. Microbiol Immunol 2004, 48:985-994.
  • [20]Stsiapura V, Sukhanova A, Artemyev M, Pluot M, Cohen JH, Baranov AV, Oleinikov V, Nabiev I: Functionalized nanocrystal-tagged fluorescent polymer beads: synthesis, physicochemical characterisation, and immunolabeling application. Anal Biochem 2004, 334:257-265.
  • [21]Lawson A, England MA: The effect of embryonic cerebrospinal fluid pressure and morphogenetic brain expansion on wound healing in the midbrain of the chick embryo. Anat Embryol (Berl) 1996, 193:601-610.
  • [22]Van Essen DC: A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997, 385:313-318.
  • [23]Hilgetag CC, Barbas H: Developmental mechanics of the primate cerebral cortex. Anat Embryol (Berl) 2005, 210:411-417.
  • [24]Lowery LA, Sive H: Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 2005, 132:2057-2067.
  • [25]Lowery LA, De Rienzo G, Gutzman JH, Sive H: Characterization and classification of zebrafish brain morphology mutants. Anat Rec (Hoboken) 2009, 292:94-106.
  • [26]Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A: New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 2006, 311:629-632.
  • [27]Pencea V, Bingaman KD, Freedman LJ, Luskin MB: Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 2001, 172:1-16.
  • [28]Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtås S, van Roon-Mom WM, Björk-Eriksson T, Nordborg C, Frisén J, Dragunow M, Faull RL, Eriksson PS: Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
  • [29]Pollay M: The function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Res 2010, 7:9.
  • [30]Goto T, Davidson L, Asashima M, Keller R: Planar cell polarity genes regulate polarized extracellular matrix deposition during frog gastrulation. Curr Biol 2005, 15:787-793.
  • [31]Luby-Phelps K, Fogerty J, Baker SA, Pazour GJ, Besharse JC: Spatial distribution of intraflagellar transport proteins in vertebrate photoreceptors. Vision Res 2008, 48:413-423.
  • [32]Burtey S, Leclerc C, Nabais E, Munch P, Gohory C, Moreau M, Fontés M: Cloning and expression of the amphibian homologue of the human PKD1 gene. Gene 2005, 357:29-36.
  • [33]Bayly R, Axelrod JD: Pointing in the right direction: new developments in the field of planar cell polarity. Nat Rev Genet 2011, 12:385-391.
  • [34]Tissir F, Goffinet AM: Planar cell polarity signaling in neural development. Curr Opin Neurobiol 2010, 20:572-577.
  • [35]Wallingford JB: Planar cell polarity signaling, cilia and polarized ciliary beating. Curr Opin Cell Biol 2010, 22:597-604.
  • [36]Guirao B, Meunier A, Mortaud S, Aguilar A, Corsi JM, Strehl L, Hirota Y, Desoeuvre A, Boutin C, Han YG, Mirzadeh Z, Cremer H, Montcouquiol M, Sawamoto K, Spassky N: Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 2010, 12:341-350.
  • [37]Hirota Y, Meunier A, Huang S, Shimozawa T, Yamada O, Kida YS, Inoue M, Ito T, Kato H, Sakaguchi M, Sunabori T, Nakaya MA, Nonaka S, Ogura T, Higuchi H, Okano H, Spassky N, Sawamoto K: Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development 2010, 137:3037-3046.
  • [38]Lametschwandtner A, Laminger A, Adam H: Development and differentiation of the brain ventricular system in tadpoles of Xenopus laevis (Daudin) (Amphibia, Anura). Z Mikrosk Anat Forsch 1983, 97:265-278.
  • [39]Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA: Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 2005, 132:1907-1921.
  • [40]Kishimoto N, Alfaro-Cervello C, Shimizu K, Asakawa K, Urasaki A, Nonaka S, Kawakami K, Garcia-Verdugo JM, Sawamoto K: Migration of neuronal precursors from the telencephalic ventricular zone into the olfactory bulb in adult zebrafish. J Comp Neurol 2011, 519:3549-3565.
  • [41]Tissir F, Qu Y, Montcouquiol M, Zhou L, Komatsu K, Shi D, Fujimori T, Labeau J, Tyteca D, Courtoy P, Poumay Y, Uemura T, Goffinet AM: Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci 2010, 13:700-707.
  文献评价指标  
  下载次数:7次 浏览次数:14次