Expression of the water-channel protein aquaporin 4 in the H-Tx rat: possible compensatory role in spontaneously arrested hydrocephalus.

OBJECT Aquaporin (AQP) water channels play an important role in water movement in the central nervous system. The authors used an animal model to examine the relationship between AQP4 expression and spontaneously arrested hydrocephalus. METHODS . Congenitally hydrocephalic H-Tx (hH-Tx) rats and nonhydrocephalic H-Tx (nH-Tx) rats were used in the study. Brain tissue sections were obtained from animals in both groups at 1 day, 1 week, 4 weeks, and 8 weeks of age. Sections were immunostained using AQP4 antibodies, and AQP4 expression was assessed. In the nH-Tx group, no AQP4 expression was seen in 1-day-old rats, and AQP4 expression was found in astrocytes around capillaries of the cerebral cortex and in ependymal cells lining the ventricles in 1-week-old rats. In the 4- and 8-week-old nH-Tx animals, AQP4 expression was seen in subpial zones of the cortex, on foot processes of pericapillary astrocytes, and in periventricular regions. A marked increase in cerebral cortical expression of AQP4 was observed at 8 weeks in the hH-Tx rats but not in the nH-Tx rats. CONCLUSIONS The authors hypothesize that the differences in cerebral AQP4 expression in the 1-day-old and 1-week-old nH-Tx rats compared with the 4- and 8-week-old nH-Tx rats may be related to the fact that the cerebrospinal fluid (CSF) circulation of newborns and infants differs from that of adults. It is also possible that the increased expression of AQP4 seen in the 8-week-old hH-Tx animals was related to the development of alternative pathways of CSF circulation, which also may occur in instances of spontaneously arrested hydrocephalus.

[1]  Geoffrey T Manley,et al.  Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. , 2004, American journal of physiology. Cell physiology.

[2]  A. Lehmenkühler,et al.  Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis , 1993, Neuroscience.

[3]  M. Brightman.  The brain's interstitial clefts and their glial walls , 2002, Journal of neurocytology.

[4]  P. Agre,et al.  Specialized Membrane Domains for Water Transport in Glial Cells: High-Resolution Immunogold Cytochemistry of Aquaporin-4 in Rat Brain , 1997, The Journal of Neuroscience.

[5]  G. Manley,et al.  Aquaporin-1 deletion reduces osmotic water permeability and cerebrospinal fluid production. , 2003, Acta neurochirurgica. Supplement.

[6]  D. Bowsher.  Pathways of absorption of protein from the cerebrospinal fluid: An autoradiographic study in the cat , 1957, The Anatomical record.

[7]  C. Granziera,et al.  Astrocyte-Specific Expression of Aquaporin-9 in Mouse Brain is Increased after Transient Focal Cerebral Ischemia , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  E. Nagelhus,et al.  Ontogeny of water transport in rat brain: postnatal expression of the aquaporin‐4 water channel , 1999, The European journal of neuroscience.

[9]  J. Frøkiaer,et al.  Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. , 2000, Biochemical and biophysical research communications.

[10]  M. Miyajima,et al.  Effect of C-type natriuretic peptide (CNP) on water channel aquaporin-4 (AQP4) expression in cultured astrocytes. , 2004, Brain research. Molecular brain research.

[11]  Peter Agre,et al.  Aquaporin water channels: molecular mechanisms for human diseases1 , 2003, FEBS letters.

[12]  A. Verkman.  Physiological importance of aquaporin water channels , 2002, Annals of medicine.

[13]  C. Epstein,et al.  Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. , 1997, The Journal of clinical investigation.

[14]  P. Agre,et al.  Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Wada.  Congenital Hydrocephalus in HTX-rats: Incidence, pathophysiology, and developmental impairment , 1988 .

[16]  B. Wiesner,et al.  Protein Kinase A Anchoring Proteins Are Required for Vasopressin-mediated Translocation of Aquaporin-2 into Cell Membranes of Renal Principal Cells* , 1999, The Journal of Biological Chemistry.

[17]  H. Cravioto,et al.  DISTRIBUTION OF INTRAVENTRICULAR HORSERADISH PEROXIDASE IN NORMAL AND HYDROCEPHALIC CAT BRAINS , 1972, Journal of Neuropathology and Experimental Neurology.

[18]  H. Reulen,et al.  Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. , 1977, Journal of neurosurgery.

[19]  K. Spring,et al.  Further characterization of the sorbitol permease in PAP-HT25 cells. , 1994, The American journal of physiology.

[20]  C. Pilgrim,et al.  Penetration and removal of horseradish peroxidase injected into the cerebrospinal fluid: Role of cerebral perivascular spaces, endothelium and microglia , 1974, Acta Neuropathologica.

[21]  P. Agre,et al.  Pathophysiology of the aquaporin water channels. , 1996, Annual review of physiology.

[22]  L. Wolfson,et al.  Pressure-dependent bulk flow of cerebrospinal fluid into brain , 1978, Experimental Neurology.

[23]  P. Agre,et al.  The aquaporin family of water channels in kidney. , 1995, Kidney international.

[24]  J. Baraban,et al.  Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  G. B. Wislocki,et al.  Absorption from the ventricles in experimentally produced internal hydrocephalus , 1921 .

[26]  T. Miyazawa,et al.  A rat model of spontaneously arrested hydrocephalus A behavioural study , 1997, Child's Nervous System.

[27]  B. Deurs.  Vesicular transport of horseradish peroxidase from brain to blood in segments of the cerebral microvasculature in adult mice , 1977, Brain Research.

[28]  E. Bering,et al.  HYDROCEPHALUS: CHANGES IN FORMATION AND ABSORPTION OF CEREBROSPINAL FLUID WITHIN THE CEREBRAL VENTRICLES. , 1963, Journal of neurosurgery.

[29]  M. Cerro.  Uptake of tracer proteins in the developing cerebellum, particularly by the growth cones and blood vessels , 1974 .

[30]  M. C. Papadopoulos,et al.  Molecular mechanisms of brain tumor edema , 2004, Neuroscience.

[31]  C. Turck,et al.  Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Marmarou,et al.  Brain edema resolution by CSF pathways and brain vasculature in cats. , 1994, The American journal of physiology.