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Expression of Dystrophins and the Dystrophin-Associated-Protein Complex by Pituicytes in Culture

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Abstract

The dystrophin-associated-protein complex (DAPC) has been extensively characterized in the central nervous system where it is localized both in neuronal and glial cells. Few studies have characterized this complex in the neurohypophysis. To further study this complex in pituicytes, the resident astroglia of the neurophypophysis, we used adult pituicyte cultures and determined the expression and localization of dystrophins/utrophins and the DAPC by RT–PCR, western blotting and immunofluorescence. Our data show that the pituicytes express dystrophins, utrophins and several members of the DAPC including dystroglycans, δ-, γ-sarcoglycans, α-dystrobrevin-1 and α1-syntrophin. Double immunofluorescence analysis shows that laminin colocalizes with dystroglycan, suggesting that similarly to muscle and astrocytes, the DAPC interacts with the extracellular matrix in pituicytes. Collectively these findings show that dystrophins/utrophins and members of the DAPC are expressed in pituicytes where they may form multiprotein complexes and play a role in the retraction-reinsertion of pituicyte endfeet during specific physiological conditions.

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References

  1. Hoffmann EP, Brown RHJ, Kunkel LM (1987) Dystrophin: the protein product of Duchenne muscular dystrophy locus. Cell 51:919–928

    Article  Google Scholar 

  2. Köenig M, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53:219–228

    Article  PubMed  Google Scholar 

  3. Köenig M, Kunkel LM (1990) Detail analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem 265:4560–4566

    PubMed  Google Scholar 

  4. Ahn AH, Kunkel LM (1993) The structural and functional diversity of dystrophin. Nat Genet 3:283–291

    Article  PubMed  CAS  Google Scholar 

  5. Mehler MF (2000) Brain dystrophin, neurogenetics and mental retardation. Brain Res Rev 32:277–307

    Article  PubMed  CAS  Google Scholar 

  6. Blake DJ, Weir A, Newey SE et al (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82:291–329

    PubMed  CAS  Google Scholar 

  7. Anderson JL, Head SI, Morley JW (2004) Long-term depression is reduced in cerebellar Purkinje cells of dystrophin-deficient mdx mice. Brain Res 1019:289–292

    Article  PubMed  CAS  Google Scholar 

  8. Vaillend C, Billard JM, Laroche S (2004) Impaired long-term spatial and recognition memory and enhanced CA1 hippocampal LTP in the dystrophin-deficient DMD (mdx) mouse. Neurobiol Disord 17:10–20

    Article  CAS  Google Scholar 

  9. Culligan KG, Makey AJ, Finn DM et al (1998) Role of dystrophin isoforms and associated proteins in muscular dystrophy. Int J Mol Med 2:639–648

    PubMed  CAS  Google Scholar 

  10. Durbeej M, Campbell KP (2002) Muscular dystrophies involving the dystrophin- glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12:349–361

    Article  PubMed  CAS  Google Scholar 

  11. Ehmsen J, Poon E, Davies K (2002) The Dystrophin-associated protein complex. J Cell Sci 115:2801–2803

    PubMed  CAS  Google Scholar 

  12. Montanaro F, Gee SH, Jacobson J et al (1998) Laminin and α-dystroglycan mediate acetylcholine receptor aggregation via MuSK-independent pathway. J Neurosci 18:1250–1260

    PubMed  CAS  Google Scholar 

  13. Jacobson C, Coté PD, Rossi SG et al (2001) The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of synaptic basement membrane. J Cell Biol 152:435–450

    Article  PubMed  CAS  Google Scholar 

  14. Russo K, Di Stasio E, Macchia G et al (2000) Characterization of β-Dystroglycan-growth factor receptor2 (Grb2) interaction. Biochem Biophys Res Comm 274:93–98

    Article  PubMed  CAS  Google Scholar 

  15. Brenman JE, Chao DS, Gee SH et al (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD95 and α1-syntrophin mediated by PDZ domains. Cell 84:757–767

    Article  PubMed  CAS  Google Scholar 

  16. Culligan K, Ohlendieck K (2002) Diversity of brain dystrophin-glycoprotein complex. J Biomed Biotechnol 2:31–36

    Article  PubMed  CAS  Google Scholar 

  17. D’Souza VN, Man N, Morris GE et al (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum Mol Genet 4:837–842

    Article  PubMed  Google Scholar 

  18. Lidov HG, Selig S, Kunkel LM (1995) Dp140: a novel 140 kDa CNS transcript from the dystrophin locus. Hum Mol Genet 4:329–335

    Article  PubMed  CAS  Google Scholar 

  19. Matsumura K, Shasby DM, Campbell KP (1993) Purification of dystrophin-related protein (utrophin) from lung and its identification in pulmonary artery endothelial cells. FEBS Lett 326:289–293

    Article  PubMed  CAS  Google Scholar 

  20. Saito F, Moore SA, Barresi R et al (2003) Unique role of dystroglycan in peripheral nerve myelination, nodal structure and sodium channel stabilization. Neuron 38:747–758

    Article  PubMed  CAS  Google Scholar 

  21. Austin RC, Howard PL, D’Souza VN et al (1995) Cloning and characterization of alternatively spliced isoforms of Dp71. Hum Mol Genet 4:1475–1483

    Article  PubMed  CAS  Google Scholar 

  22. Austin RC, Morris GE, Howard PL et al (2000) Expression and synthesis of alternatively spliced variants of Dp71 in adult humain brain. Neuromuscul Disord 10:187–193

    Article  PubMed  CAS  Google Scholar 

  23. Blake DJ, Hawkes R, Benson MA et al (1999) Different dystrophin-like complexes are expressed in neurons and glia. J Cell Biol 147:645–658

    Article  PubMed  CAS  Google Scholar 

  24. Ibraghimov-Breskovnaya O, Ervasti JM, Leveille CJ et al (1992) Primary structure of dystrophin-associated glycoprotein linking dystrophin to the extracellular matrix. Nature 355:696–702

    Article  Google Scholar 

  25. Henry MD, Campbell KP (1999) Dystroglycan inside and out. Curr Opin Cell Biol 11:602–607

    Article  PubMed  CAS  Google Scholar 

  26. Blake DJ, Kröger S (2000) The neurobiology of Duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci 23:92–99

    Article  PubMed  CAS  Google Scholar 

  27. Dorbani-Mamine L, Stoekel ME, Janscik V et al (1998) Dystrophin in neurohypophysial lobe of normal and dehydrated rats: immunolocalization and biochemical characterization. Neuroreport 9:3583–3587

    Article  PubMed  CAS  Google Scholar 

  28. Benabdesselam R, Sene A, Raison D et al (2010) A deficit of brain dystrophin Dp71 impairs hypothalamic osmostat. J Neurosci Res 88:324–334

    Article  PubMed  CAS  Google Scholar 

  29. Claudepierre T, Rodius F, Frasson M et al (1999) Differential distribution of dystrophins in rat retina. Invest Ophthalmol Vis Sci 40:1520–1529

    PubMed  CAS  Google Scholar 

  30. Satz JS, Ostendorf AP, Hou S et al (2010) Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci 30:14560–14572

    Article  PubMed  CAS  Google Scholar 

  31. Ramsell D, Zhao BG, Baker D et al (1996) Serum modulates cyclic AMP-dependent morphological changes cultured neurohypophysial astrocytes. Brain Res Bull 39:109–114

    Article  PubMed  CAS  Google Scholar 

  32. Fabbrizio E, Bonet-Kerrache A, Leger JJ et al (1993) Actin-Dystrophin interface. Biochemistry 32:10457–10463

    Article  PubMed  CAS  Google Scholar 

  33. Rivier F, Robert A, Hugon G et al (1999) Dystrophin and utrophin complexed with different associated proteins in cardiac Purkinje fibers. Histochem J 31:425–432

    Article  PubMed  CAS  Google Scholar 

  34. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanat-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  35. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principe of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  36. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from poly-acrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4353

    Article  PubMed  CAS  Google Scholar 

  37. Lidov HG, Byers TJ, Kunkel LM (1993) The distribution of dystrophin in the murine central nervous system: an immunocytochemical study. Neuroscience 54:167–187

    Article  PubMed  CAS  Google Scholar 

  38. Imamura M, Ozawa E (1998) Differential expression of dystrophin isoforms and utrophin during dibutyryl-cAMP-induced morphological differentiation of rat brain astrocytes. Proc Natl Acad Sci USA 95:6139–6144

    Article  PubMed  CAS  Google Scholar 

  39. Villarreal-Silva M, Suárez-Sánchez R, Rodríguez-Muñoz R et al (2010) Dystrophin Dp71 is critical for stability of the DAPs in the nucleus of PC12 cells. Neurochem Res 35:366–373

    Article  PubMed  CAS  Google Scholar 

  40. Ritz K, van Schaik BD, Jakobs ME et al (2011) SGCE isoform characterization and expression in human brain: implications for myoclonus-dystonia pathogenesis? Eur J Hum Genet 19:438–444

    Article  PubMed  CAS  Google Scholar 

  41. Waite A, Tinsley CL, Locke M et al (2009) The neurobiology of the dystrophin-associated glycoprotein complex. Ann Med 41:344–359

    Article  PubMed  CAS  Google Scholar 

  42. Moukhles H, Roque R, Carbonetto S (2000) Alpha-dystroglycan isoforms are differentially distributed in adult rat retina. J Comp Neurol 420:182–194

    Article  PubMed  CAS  Google Scholar 

  43. Henry MD, Campbell KP (1996) Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 8:625–631

    Article  PubMed  CAS  Google Scholar 

  44. Claudepierre T, Mornet D, Pannicke T et al (2000) Expression of Dp71 in Müller glial cells: a comparison with utrophin and dystrophin associated proteins. Invest Ophtalmol Vis Sci 41:294–304

    CAS  Google Scholar 

  45. Blank M, Blake DJ, Kröger S (2002) Molecular diversity of the dystrophyn-like protein complex in the developing and adult avian retina. Neuroscience 111:259–273

    Article  PubMed  CAS  Google Scholar 

  46. Claudepierre T, Dalloz C, Mornet D et al (2000) Characterization of the intermolecular association of dystrophin-associated glycoprotein complex in retinal Müller glial cells. J Cell Sci 113:3409–3417

    PubMed  CAS  Google Scholar 

  47. Garcia-Tovar CG, Luna J, Mena R et al (2002) Dystrophin isoform Dp71 is present in lamellipodia and focal complexes in human astrocytoma cells U-373 MG. Acta Histochem 104:245–254

    Article  PubMed  CAS  Google Scholar 

  48. Cerna J, Cerecedo D, Ortega A et al (2006) Dystrophin Dp71f associates with the beta1-integrin adhesion complex to modulate PC12 cell adhesion. J Mol Biol 362:954–965

    Article  PubMed  CAS  Google Scholar 

  49. Libby RT, Champliaud MF, Claudepierre T et al (2000) Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci 20:6517–6528

    PubMed  CAS  Google Scholar 

  50. Roediger M, Miosge N, Gersdorff N (2010) Tissue distribution of the laminin beta1 and beta2 chain during embryonic and fetal human development. J Mol Histol 41:177–184

    Article  PubMed  CAS  Google Scholar 

  51. Kuwahara S, Maeda S, Ardiles Y et al (2010) Immunohistochemical localization of aquaporin-4 in the rat pituitary gland. J Vet Med Sci 72:1307–1312

    Article  PubMed  CAS  Google Scholar 

  52. Neely JD, Amiry-Moghaddam M, Otterson OP et al (2001) Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc Natl Acad Sci USA 98:14108–14113

    Article  PubMed  CAS  Google Scholar 

  53. Dalloz C, Sarig R, Fort P et al (2003) Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mousse retina. Hum Mol Genet 12:1543–1554

    Article  PubMed  CAS  Google Scholar 

  54. Fort P, Sene A, Pannicke T et al (2008) Kir4.1 and AQP4 associate with Dp71- and utrophin-DAPs complexes in specific and defined microdomains of Müller retinal glial cell membrane. Glia 56:597–610

    Article  PubMed  Google Scholar 

  55. Amiry-Moghaddam M, Otsuka T, Hurn PD et al (2003) An α-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci USA 100:2106–2111

    Article  PubMed  CAS  Google Scholar 

  56. Guadagno E, Moukhles H (2004) Laminin-induced aggregation of inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via dystroglycan-containing complex in astrocytes. Glia 47:138–149

    Article  PubMed  Google Scholar 

  57. Noël G, Tham DKL, Moukhles H (2009) Interdependence of laminin-mediated clustering of lipid rafts and dystroglycan complex in astrocytes. J Biol Chem 284:19694–19704

    Article  PubMed  Google Scholar 

  58. Perlmutter LS, Hatton GI, Tweedle CD (1984) Plasticity in the neurohypophysis in vitro: effects of osmotic changes on pituicytes. Neuroscience 12:503–511

    Article  PubMed  CAS  Google Scholar 

  59. Tweedle CD, Hatton GI (1987) Morphological adaptability at neurosecretory axonal endings on the neurovascular contact zone of the rat neurohypophysis. Neuroscience 20:241–246

    Article  PubMed  CAS  Google Scholar 

  60. Luckman SM, Bicknell RJ (1990) Morphological plasticity that occurs in the neuro hypophysis following activation of magnocellular neurosecretory system can be mimicked in vitro by β-adrenergic stimulation. Neuroscience 39:701–709

    Article  PubMed  CAS  Google Scholar 

  61. Miyata S, Furuya K, Nakai S et al (1999) Morphological plasticity and rearrangement of cytoskeletons in pituicytes cultured from adult rat neurohypophysis. Neurosci Res 33:299–306

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are very grateful to Dr H Moukhles for the critical review and extensive editing of the paper. They would like also to thank Professor Sahel, director of the Institut de la Vision in Paris for hosting Bougrid Abdelkader. This project was supported by the Algerian « Ministère de l’Enseignement Supérieur et de la Recherche Scientifique » and the French « Ministère des Affaires Etrangères et Européennes » .

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Authors and Affiliations

  1. Laboratoire de Biologie et Physiologie des Organismes, Faculté des Sciences Biologiques, Université des Sciences et de la Technologie Houari Boumédienne (USTHB), Algiers, Algeria

    Abdelkader Bougrid, Ghazi Ayad & Latifa Dorbani-Mamine

  2. Department of Ophtalmology and Eye Hospital, Faculty of Medicine, University of Leipzig, Liebigstrasse 10-14, 04103, Leipzig, Germany

    Thomas Claudepierre

  3. INSERM, U968, 75012, Paris, France

    Serge Picaud & Alvaro Rendon

  4. UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, 17 rue Moreau, 75012, Paris, France

    Serge Picaud & Alvaro Rendon

  5. CNRS, UMR_7210, 75012, Paris, France

    Serge Picaud & Alvaro Rendon

  6. Département de Physiologie des Interactions (EA701), Institut de Biologie, Bvd Henry IV, 34062, Montpellier, France

    Dominique Mornet

  7. Laboratoire Microenvironnements et Comportements Cellulaires, Département de Biologie, Université de Cergy-Pontoise, 2, rue Adolphe Chauvin, BP 222, 95302, Cergy-Pontoise Cedex, France

    Halima Darbeida

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  1. Abdelkader Bougrid
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  2. Thomas Claudepierre
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  3. Serge Picaud
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  4. Ghazi Ayad
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  5. Dominique Mornet
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  6. Latifa Dorbani-Mamine
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Correspondence to Halima Darbeida.

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This paper is dedicated to the memory of the late Pr Ghazi Ayad.

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Bougrid, A., Claudepierre, T., Picaud, S. et al. Expression of Dystrophins and the Dystrophin-Associated-Protein Complex by Pituicytes in Culture. Neurochem Res 36, 1407–1416 (2011). https://doi.org/10.1007/s11064-011-0466-6

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