Platelet adhesion: Structural and functional diversity of short dystrophin and utrophins in the formation of dystrophinassociated-protein complexes related to actin dynamics

Doris Cerecedo; Dalila Martínez-Rojas; Oscar Chávez; Francisco Martínez-Pérez; Francisco García-Sierra; Álvaro Rendon; Dominique Mornet; Ricardo Mondragón

doi:10.1160/TH04-11-0765

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2005; 94(06): 1203-1212
DOI: 10.1160/TH04-11-0765

Platelets and Blood Cells

Schattauer GmbH

Platelet adhesion: Structural and functional diversity of short dystrophin and utrophins in the formation of dystrophinassociated-protein complexes related to actin dynamics

Authors

Doris Cerecedo^*

¹Departamento Bioquímica, CINVESTAV, D.F., México
Dalila Martínez-Rojas

²Departamento Fisiología, Biofísica y Neurociencias, CINVESTAV
Oscar Chávez

²Departamento Fisiología, Biofísica y Neurociencias, CINVESTAV
Francisco Martínez-Pérez

²Departamento Fisiología, Biofísica y Neurociencias, CINVESTAV
Francisco García-Sierra

³Departamento Biología Celular, CINVESTAV, México
Álvaro Rendon

⁴Laboratoire de Physiopathologie Cellulaire et Moléculaire de la Rétine, INSERM-U592, Hopital Saint-Antoine, Paris, France
Dominique Mornet

⁵Muscles et Pathologies Chroniques, Institut de Biologie, Montpellier, France
Ricardo Mondragón

¹Departamento Bioquímica, CINVESTAV, D.F., México

Abstract

Summary

Platelets are dynamic cell fragments that modify their shape during activation. Utrophin and dystrophins are minor actin-binding proteins present in muscle and non-muscle cytoskeleton. In the present study, we characterised the pattern of Dp71 isoforms and utrophin gene products by immunoblot in human platelets. Two new dystrophin isoforms were found, Dp71f and Dp71d, as well as the Up71 isoform and the dystrophin-associated proteins, α and β-dystrobrevins. Distribution of Dp71d/Dp71Δ₁₁₀ ^m, Up400/Up71 and dystrophin-associated proteins in relation to the actin cytoskeleton was evaluated by confocal microscopy in both resting and platelets adhered on glass. Formation of two dystrophin-associated protein complexes (Dp71d/Dp71Δ₁₁₀ ^m ~DAPC and Up400/Up71~DAPC) was demonstrated by co-immunoprecipitation and their distribution in relation to the actin cytoskeleton was characterised during platelet adhesion. The Dp71d/Dp71Δ₁₁₀ ^m ~DAPC is maintained mainly at the granulomere and is associated with dynamic structures during activation by adhesion to thrombin-coated surfaces. Participation of both Dp71d/Dp71Δ₁₁₀ ^m ~DAPC and Up400/Up71~DAPC in the biological roles of the platelets is discussed.

Keywords

Actin structures - adhesion - cytoskeleton - dystrophin-associated protein complexes - platelet activation

Full Text

References

References
1 Lewis JC, White MS, Prater T. et al Three-dimensional organizations of the platelet cytoskeleton during adhesion in vitro: observations on human and non human primates cells. Cell Motil 1983; 3: 589-608.
2 White JG. Fine structural alterations induced in platelets by adenosine diophosphate. Blood 1968; 31: 604-22.
3 Nachmias VT. Cytoskeleton of human platelets at rest and after spreading. J Cell Biol 1980; 86: 795-802.
4 Flaumenhaft R. Molecular basis of platelet granule secretion. Arterioscler Thromb Vasc Biol 2003; 23: 1152-60.
5 Israels SJ, Gerrard JM, Jacques YV. et al Platelet dense granule membranes contain both granulophysin and P-selectin (GMP-140). Blood 1992; 80: 143-52.
6 Youssefian T, Masse JM, Rendu F. et al Platelet and megakaryocyte dense granules contain glycoproteins Ib and IIb-IIIa. Blood 1997; 89: 4047-57.
7 Hartwig JH. Mechanisms of actin rearrangements mediating platelet activation. J Cell Biol 1992; 118: 1431-42.
8 Allen RD, Zacharaski LR, Widirstky ST. et al Transformation and motility of human platelets. Details of the shape change and release reaction observed by optical and electron microscopy. J Cell Biol 1979; 83: 126-42.
9 Bearer EL. Cytoskeletal domains in the activated platelet. Cell Motil Cytoskeleton 1995; 30: 50-66.
10 Debus E, Weber K, Osborn M. The cytoskeleton of blood platelets viewed by immunofluorescence microscopy. Eur J Cell Biol 1981; 24: 45-52.
11 Sixma JJ, van der Berg A, Jockusch BM. et al Immunolelectron microscopy localization of actin, α-actinin, actin-binding protein and myosin in resting and activated human blood platelets. Eur J Cell Biol 1989; 48: 271-81.
12 Takubo T, Hino M, Suzuki k. et al Localization of myosin, actin, α-actinin, tropomyosin and vinculin in surface-activated, spreading human platelets. Biothec Histoch 1998; 73: 310-5.
13 Bearer EL, Prakash JM, Li Z. Actin dynamics in platelets. Int Rev Cytol 2002; 217: 137-81.
14 Flaumenhaft R, Dilks JR, Rozenvayn N. et al The actin cytoskeleton differentially regulates platelet α-granule and dense granule secretion. Blood 2005; 105: 3879-87.
15 Hartwig JH. Introduction and subfamily 1: the spectrin family. In: Sheterline p. (Ed) Protein profile, actin-binding proteins spectrin superfamily. Academic Press; London, UK: 1994: 711-49.
16 Bar S, Barnea E, Levy Z. et al A novel product of the Duchenne muscular dystrophy gene which greatly differs from known isoforms in its structure and tissue distribution. Biochem J 1990; 272: 557-60.
17 Górecki DC, Monaco AP, Derry JMJ. et al Expression of four alternative dystrophin transcripts in brain regions regulated by different promoters. Mol Genetics 1992; 1: 505-10.
18 Rapaport D, Greenberg DS, Tal M. et al Dp71, the non-muscle product of the Duchenne muscular dystrophy gene is associated with the cell membrane. FEBS Lett 1993; 328: 197-202.
19 Byers TJ, Lidov HG, Kunkel LM. An alterative dystrophin transcript specific to peripheral nerve. Nat Genet 1993; 4: 77-81.
20 D’Souza VN, Nguyen TM, Morris GE. et al A novel dystrophin isoform is required for normal retinal electrophysiology. Hum Mol Gen 1995; 4: 837-42.
21 Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille J. et al Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 1992; 355: 696-702.
22 Ervasti JM, Campbell KP. A role for the dystrophinglycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 1993; 122: 809-23.
23 Crawford GE, Faulkner JA, Crosbie RH. et al Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 1992; 150: 1399-409.
24 Claudepierre T, Mornet D, Pannicke T. et al Expression of Dp71 in Muller glial cells: a comparison with utrophin- and dystrophin-associated proteins. Invest Ophtal Visual Sci 2000; 41: 294-304.
25 Hernández-González EO, Martínez-Rojas D, Mornet D. et al Comparative distribution of short dystrophin superfamily products in various guinea pig spermatozoa domains. Eur J Cell Biol 2001; 80: 792-8.
26 García-Tovar CG, Luna J, Mena R. et al Dystrophin isoform Dp71 is present in lamellipodia and focal complexes in human astrocytoma cells U-373 MG. Acta Histochem 2002; 104: 245-54.
27 Earnest JP, Santos GF, Zuerbig S. et al Dystrophinrelated protein in the platelet membrane skeleton. Integrin-induced change in detergent-insolubility and cleavage by calpain in aggregating platelets. J Biol Chem 1995; 270: 27259-65.
28 Austin RC, Fox JEB, Werstuck GH. et al Identification of Dp71 isoforms in the platelet membrane cytoskeleton. Potential role in thrombin-mediated platelet adhesion. J Biol Chem 2002; 277: 47106-13.
29 Austin RC, Howard PL, D’Souza VN. et al Cloning and characterization of alternatively spliced isoforms of Dp71. Hum Mol Genet 1995; 4: 1475-83.
30 Khurana TS, Hoffman EP, Kunkel LM. Identification of a chromosome 6 encoded dystrophin-related protein. J Biol Chem 1990; 265: 16717-20.
31 Wilson J, Putt W, Jiménez C. et al Up71 and Up140, two novel transcripts of utrophin that are homologues of short forms of dystrophin. Hum Mol Gen 1999; 8: 1271-8.
32 Winder SJ, Hemmings L, Maciver SK. et al Utrophin actin binding domain: analysis of actin binding and cellular targeting. J Cell Sci 1995; 108: 63-71.
33 James M, thi Man, Nguyen Wise CJ. et al Utrophin-dystroglycan complex in membranes of adherent cultured cells. Cell Motil Cytoskeleton 1996; 33: 163-74.
34 Moores CA, Kendrick-Jones J. Biochemical characterisation of the actin-binding properties of utrophin. Cell Motil Cytoskeleton 2000; 46: 116-28.
35 Cerecedo D, Stock R, González S. et al Modification of actin, myosin and tubulin distribution during cytoplasmic granule movements associated with platelet adhesion. Heamotologica 2002; 87: 1165-76.
36 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-5.
37 Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidium trhiocyanate-phenolchloroform extraction. Anal Biochem 1987; 162: 156-9.
38 Austin RC, Morris GE, Howard PL. et al Expression and synthesis of alternatively spliced variants of Dp71 in adult human brain. Neuromusc Disord 2000; 10: 187-93.
39 Blake DJ, Tinsley JM, Davies KE. The emerging family of dystrophin-related proteins. Trends Cell Biol 1994; 4: 19-23.
40 Holzfeind PJ, Ambrose HJ, Newey SE. et al Tissueselective expression of α-dystrobrevin is determined by multiple promotors. J Biol Chem 1999; 274: 6250-8.
41 Howard PL, Klamut HJ, Ray PN. Identification of a novel actin binding site within the Dp71 dystrophin isoform. FEBS Lett 1998; 441: 337-41.
42 Cheng YJ, Spence HJ, Cameron JM. et al Direct interaction of beta-dystroglycan with F-actin. Biochem J 2003; 375: 329-37.
43 Kulyte A, Navakauskiene R, Treigyte G. et al Characterization of human promyelocytic leukemia cells undergoing granulocytic differentiation. Mol Biol Cell 2002; 13: 4195-205.
44 Dalloz C, Sarig R, Fort P. et al Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum Mol Genet 2003; 12: 1543-54.
45 Tinsley JM, Potter AC, Phelps SR. et al Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 1996; 384: 349-53.
46 Hernandez-Gonzalez EO, Mornet D, Rendon A. et al Abscence of Dp71 in mdx3cv mouse spermatozoa alters flagellar morphology and the distribution of ion channels and nNOS. J Cell Sci 2005; 118: 137-45.
47 Adams ME, Mueller HA, Froehner SC. In vivo requirement of the α-syntrophin PDZ domain for the sarcolemmal localization of nNOS and aquaporin-4. J Cell Biol 2001; 155: 113-22.
48 Forst J, Forst R, Leithe H. et al Platelet function deficiency in Duchenne muscular dystrophy. Neuromusc Disord 1998; 8: 46-9.
49 Baydur A, Kanel G. Tracheobronchomalacia and tracheal hemorrhage in patients with Duchenne muscular dystrophy receiving long-term ventilation with uncuffed trhacheostomies. Chest 2003; 123: 1307-11.
50 Turturro F, Rocca B, Gumina S. et al Impaired primary hemostasis with normal platelet function in Duchenne muscular dystrophy during highly-invasive spinal surgery. Nueromusc Disord 2005; 15: 532-40.