Biological activities and molecular interactions of the C-terminal residue of thrombospondin-4, an epitome of acidic amphipathic peptides

Peptides

Volumn 31, Issue 4, 2010, Pages 723-735

  Congote, Luis F ^a   Sadvakassova, Gulzhakhan ^a   Dobocan, Monica C ^a   DiFalco, Marcos R ^b   Kriazhev, Leonid ^b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cell penetrating peptide; DNA replication; Hepatitis C virus; Integrins; NS5A; Papillomavirus; Posttranscriptional regulation; RNA recognition motifs; ROD1; STAT3; Transcriptional activator E2

Indexed keywords

CD47 ANTIGEN; DYNACTIN; ERYTHROID POTENTIATING FACTOR; ERYTHROPOIETIN; HERMES ANTIGEN; MATRIX PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 5; NUCLEAR PROTEIN; OSTEOPONTIN; PEPTIDE DERIVATIVE; THROMBOSPONDIN; THROMBOSPONDIN 1; THROMBOSPONDIN 4; TRITON X 100; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANEMIA; BIOLOGICAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CELL NUCLEUS; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); ENDOTHELIUM CELL; ERYTHROCYTE SHAPE; HEMATOPOIETIC STEM CELL; HUMAN; KIDNEY EPITHELIUM; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SKIN FIBROBLAST;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD44; CELL ADHESION MOLECULES; CELL MEMBRANE; CELL NUCLEUS; CHROMATOGRAPHY, AFFINITY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SURFACE-ACTIVE AGENTS; THROMBOSPONDINS;

HEPATITIS C VIRUS; MUS; PAPILLOMAVIRIDAE;

EID: 77649233730     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2009.12.011     Document Type: Review

References (130)

1. Adams J.C., and Lawler J. The thrombospondins. Int J Biochem Cell Biol 36 (2004) 961-968
2. Adkins J.N., Varnum S.M., Auberry K.J., Moore R.J., Angell N.H., Smith R.D., et al. Toward a human blood serum proteome: analysis by multidimensional separation coupled with mass spectrometry. Mol Cell Proteomics 1 (2002) 947-955
3. Ahn J., Chung K.S., Kim D.U., Won M., Kim L., Kim K.S., et al. Systematic identification of hepatocellular proteins interacting with NS5A of the hepatitis C virus. J Biochem Mol Biol 37 (2004) 741-748
4. Anagnostou A., Lee E.S., Kessimian N., Levinson R., and Steiner M. Erythropoietin has a mitogenic and positive chemotactic effect on endothelial cells. Proc Natl Acad Sci USA 87 (1990) 5978-5982
5. Antson A.A., Burns J.E., Moroz O.V., Scott D.J., Sanders C.M., Bronstein I.B., et al. Structure of the intact transactivation domain of the human papillomavirus E2 protein. Nature 403 (2000) 805-809
6. Arai F., Hirao A., and Suda T. Regulation of hematopoietic stem cells by the niche. Trends Cardiovasc Med 15 (2005) 75-79
7. Avigdor A., Goichberg P., Shivtiel S., Dar A., Peled A., Samira S., et al. CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to the bone marrow. Blood 103 (2004) 2981-2989
8. Bajorath J., and Molecular Organization. Structural features, and ligand binding characteristics of Cd44, a highly variable cell surface glycoprotein with multiple functions. Proteins-Struct Funct Genet 39 (2000) 103-111
9. Baker L.H., Rowinsky E.K., Mendelson D., Humerickhouse R.A., Knight R.A., Qian J., et al. Randomized, phase II study of the thrombospondin-1-mimetic angiogenesis inhibitor ABT-510 in patients with advanced soft tissue sarcoma. J Clin Oncol 26 (2008) 5583-5588
10. Barlow D.J., and Thornton J.M. Helix geometry in proteins. J Mol Biol 201 (1988) 601-619
11. Baxter M.K., and McBride A.A. An acidic amphipathic helix in the bovine papillomavirus E2 protein is critical for DNA replication and interaction with the E1 protein. Virology 332 (2005) 78-88
12. Bechinger B. Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J Membr Biol 156 (1997) 197-211
13. Benaud C., Gentil B.J., Assard N., Court M., Garin J., Delphin C., et al. AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture. J Cell Biol 164 (2004) 133-144
14. Billups D., Hanley J.G., Orme M., Attwell D., and Moss S.J. GABAC receptor sensitivity is modulated by interaction with MAP1B. J Neurosci 20 (2000) 8643-8650
15. Bonanno G., Mariotti A., Procoli A., Corallo M., Rutella S., Pessina G., et al. Human cord blood CD133+ cells immunoselected by a clinical-grade apparatus differentiate in vitro into endothelial- and cardiomyocyte-like cells. Transfusion 47 (2007) 280-289
16. Bonnefoy A., and Legrand C. Proteolysis of subendothelial adhesive glycoproteins (fibronectin, thrombospondin, and von Willebrand factor) by plasmin, leukocyte cathepsin G, and elastase. Thromb Res 98 (2000) 323-332
17. Bonnefoy A., Moura R., and Hoylaerts M.F. Thrombospondins: from structure to therapeutics-the evolving role of thrombospondin-1 in hemostasis and vascular biology. Cell Mol Life Sci 65 (2008) 713-727
18. Borgonovo B., Cocucci E., Racchetti G., Podini P., Bachi A., and Meldolesi J. Regulated exocytosis: a novel, widely expressed system. Nat Cell Biol 4 (2002) 955-962
19. Boutz P.L., Chawla G., Stoilov P., and Black D.L. MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes Dev 21 (2007) 71-84
20. Boutz P.L., Stoilov P., Li Q., Lin C.H., Chawla G., Ostrow K., et al. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21 (2007) 1636-1652
21. Brass V., Bieck E., Montserret R., Wolk B., Hellings J.A., Blum H.E., et al. An Amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J Biol Chem 277 (2002) 8130-8139
22. Brines M., and Cerami A. Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J Intern Med 264 (2008) 405-432
23. Brown E.J., and Frazier W.A. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11 (2001) 130-135
24. Cal S., Arguelles J.M., Fernandez P.L., and Lopez-Otin C. Identification, characterization, and intracellular processing of ADAM-TS12, a novel human disintegrin with a complex structural organization involving multiple thrombospondin-1 repeats. J Biol Chem 276 (2001) 17932-17940
25. Chen H., Herndon M.E., and Lawler J. The cell biology of thrombospondin-1. Matrix Biol 19 (2000) 597-614
26. Cho N.J., Cheong K.H., Lee C., Frank C.W., and Glenn J.S. Binding dynamics of hepatitis C virus′ NS5A amphipathic peptide to cell and model membranes. J Virol 81 (2007) 6682-6689
27. Chung J., Gao A.G., and Frazier W.A. Thrombospondin acts via integrin-associated protein to activate the platelet integrin alphaIIbbeta3. J Biol Chem 272 (1997) 14740-14746
28. Congote L.F., Difalco M.R., and Gibbs B.F. The C-terminal peptide of thrombospondin-4 stimulates erythroid cell proliferation. Biochem Biophys Res Commun 324 (2004) 673-678
29. Congote L.F., and DiFalco M.R. Gibbs BF. Thrombospondin 1, produced by endothelial cells under the action of erythropoietin, stimulates thymidine incorporation into erythroid cells and counteracts the inhibitory action of insulin-like growth factor binding protein 3. Cytokine 30 (2005) 248-253
30. Dave B., and Chang J. Treatment resistance in stem cells and breast cancer. J Mam Gland Biol Neoplasia 14 (2009) 79-82
31. Detwiler T.C., Turk J.L., and Browne P.C. Thiol-disulfide exchange by thrombospondin. Semin Thromb Hemost 13 (1987) 276-280
32. Dickinson S.C., Vankemmelbeke M.N., Buttle D.J., Rosenberg K., Heinegard D., and Hollander A.P. Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol 22 (2003) 267-278
33. DiFalco M.R., and Congote L.F. Antagonism between interleukin 3 and erythropoietin in mice with azidothymidine-induced anemia and in bone marrow endothelial cells. Cytokine 18 (2002) 51-60
34. Dimitroff C.J., Lee J.Y., Rafii S., Fuhlbrigge R.C., and Sackstein R. CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 153 (2001) 1277-1286
35. Dobocan M., and Sadvakassova G. Congote LF. Chaperonin 10 as an endothelial-derived differentiation factor: role of glycogen synthase kinase-3. J Cell Physiol 219 (2009) 470-476
36. Dohner K., Wolfstein A., Prank U., Echeverri C., Dujardin D., Vallee R., et al. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol Biol Cell 13 (2002) 2795-2809
37. Donnini S., Morbidelli L., Taraboletti G., and Ziche M. ERK1-2 and p38 MAPK regulate MMP/TIMP balance and function in response to thrombospondin-1 fragments in the microvascular endothelium. Life Sci 74 (2004) 2975-2985
38. Elazar M., Cheong K.H., Liu P., Greenberg H.B., Rice C.M., and Glenn J.S. Amphipathic helix-dependent localization of NS5A mediates hepatitis C virus RNA replication. J Virol 77 (2003) 6055-6061
39. Floquet N., Dedieu S., Martiny L., Dallchez M., Perahia D., and Human Thrombospondin's. (Tsp-1) C-terminal domain opens to interact with the Cd-47 receptor: a molecular modeling study. Arch Biochem Biophys 478 (2008) 103-109
40. Garrett R.W., and Emerson S.G. The role of parathyroid hormone and insulin-like growth factors in hematopoietic niches: physiology and pharmacology. Mol Cell Endocrinol 288 (2008) 6-10
41. Gassmann M., Heinicke K., Soliz J., Ogunshola O.O., Marti H.H., Hofer T., et al. Non-erythroid functions of erythropoietin. Adv Exp Med Biol 543 (2003) 323-330
42. Giniger E., and Ptashne M. Transcription in yeast activated by a putative amphipathic alpha helix linked to a DNA binding unit. Nature 330 (1987) 670-672
43. Gordon M.S., Mendelson D., Carr R., Knight R.A., and Humerickhouse R.A. Iannone Mand Stopeck AT. A phase 1 trial of 2 dose schedules of ABT-510, an antiangiogenic, thrombospondin-1-mimetic peptide, in patients with advanced cancer. Cancer 113 (2008) 3420-3429
44. Gotis-Graham I., Hogg P.J., and McNeil H.P. Significant correlation between thrombospondin 1 and serine proteinase expression in rheumatoid synovium. Arthritis Rheum 40 (1997) 1780-1787
45. Greenaway J., Henkin J., Lawler J., Moorehead R., and Petrik J. ABT-510 induces tumor cell apoptosis and inhibits ovarian tumor growth in an orthotopic, syngeneic model of epithelial ovarian cancer. Mol Cancer Ther 8 (2009) 64-74
46. Haase H., and Ahnak. a new player in beta-adrenergic regulation of the cardiac L-type Ca2+ channel. Cardiovasc Res 73 (2007) 19-25
47. Haase H., Podzuweit T., Lutsch G., Hohaus A., Kostka S., Lindschau C., et al. Signaling from beta-adrenoceptor to L-type calcium channel: identification of a novel cardiac protein kinase A target possessing similarities to AHNAK. FASEB J 13 (1999) 2161-2172
48. Harris D., Zhang Z., Chaubey B., and Pandey V.N. Identification of cellular factors associated with the 3′-nontranslated region of the hepatitis C virus genome. Mol Cell Proteom 5 (2006) 1006-1018
49. Hashimoto T., Gamou S., Shimizu N., Kitajima Y., and Nishikawa T. Regulation of translocation of the desmoyokin/AHNAK protein to the plasma membrane in keratinocytes by protein kinase C. Exp Cell Res 217 (1995) 258-266
50. Haylock D.N., and Nilsson S.K. The role of hyaluronic acid in hemopoietic stem cell biology. Regenerat Med 1 (2006) 437-445
51. Hogg P.J. Thrombospondin 1 as an enzyme inhibitor. Thromb Haemost 72 (1994) 787-792
52. Hogg P.J., Jimenez B.M., and Chesterman C.N. Identification of possible inhibitory reactive centers in thrombospondin 1 that may bind cathepsin G and neutrophil elastase. Biochemistry 33 (1994) 6531-6537
53. Hogg P.J., Owensby D.A., Mosher D.F., Misenheimer T.M., and Chesterman C.N. Thrombospondin is a tight-binding competitive inhibitor of neutrophil elastase. J Biol Chem 268 (1993) 7139-7146
54. Hope I.A., Mahadevan S., and Struhl K. Structural and functional characterization of the short acidic transcriptional activation region of yeast GCN4 protein. Nature 333 (1988) 635-640
55. Hornebeck W., Emonard H., Monboisse J.C., and Bellon G. Matrix-directed regulation of pericellular proteolysis and tumor progression. Semin Cancer Biol 12 (2002) 231-241
56. Huttelmaier S., Illenberger S., Grosheva I., Rudinger M., Singer R.H., and Jockusch B.M. Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J Cell Biol 155 (2001) 775-785
57. Iwata T., Lee S., Oishi O., Aoyagi H., Ohno M., Anzai K., et al. Design and synthesis of amphipathic 3(10)-helical peptides and their interactions with phospholipid bilayers and ion channel formation. J Biol Chem 269 (1994) 4928-4933
58. Jacobson K., and Dietrich C. Looking at lipid rafts?. Trends Cell Biol 9 (1999) 87-91
59. Kadonaga J.T. Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell 116 (2004) 247-257
60. Kang J.A., Zhou Y., Weis T.L., Liu H., Ulaszek J., Satgurunathan N., et al. Osteopontin regulates actin cytoskeleton and contributes to cell proliferation in primary erythroblasts. J Biol Chem 283 (2008) 6997-7006
61. Katayama Y., Battista M., Kao W.M., Hidalgo A., Peired A.J., Thomas S.A., et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124 (2006) 407-421
62. Kawano Y., Kobune M., Chiba H., Nakamura K., Takimoto R., Takada K., et al. Ex vivo expansion of G-CSF-mobilized peripheral blood CD133+ progenitor cells on coculture with human stromal cells. Exp Hematol 34 (2006) 150-158
63. Kiel M.J., and Morrison S.J. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8 (2008) 290-301
64. Kosfeld M.D., and Frazier W.A. Identification of a new cell adhesion motif in two homologous peptides from the COOH-terminal cell binding domain of human thrombospondin. J Biol Chem 268 (1993) 8808-8814
65. Kvansakul M., Adams J.C., and Hohenester E. Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J 23 (2004) 1223-1233
66. Larsson E., Harris H.E., Larsson A., Mansson B., Saxne T., and Klareskog L. corticosteroid treatment of experimental arthritis retards cartilage destruction as determined by histology and serum. Compr Rheumatol 43 (2004) 428-434
67. Lawler J., Derick L.H., Connolly J.E., Chen J.H., and Chao F.C. The structure of human platelet thrombospondin. J Biol Chem 260 (1985) 3762-3772
68. Lee I.H., Lim H.J., Yoon S., Seong J.K., Bae D.S., Rhee S.G., et al. Ahnak protein activates protein kinase C (PKC) through dissociation of the PKC-protein phosphatase 2A complex. J Biol Chem 283 (2008) 6312-6320
69. Lee J.L., Wang M.J., and Chen J.Y. Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J Cell Biol 185 (2009) 949-957
70. Lee J.L., Wang M.J., Sudhir P.R., Chen G.D., Chi C.W., and Chen J.Y. Osteopontin promotes integrin activation through outside-in and inside-out mechanisms: OPN-CD44V interaction enhances survival in gastrointestinal cancer cells. Cancer Res 67 (2007) 2089-2097
71. Lee J.L., Wang M.J., Sudhir P.R., and Chen J.Y. CD44 engagement promotes matrix-derived survival through the CD44-SRC-integrin axis in lipid rafts. Mol Cell Biol 28 (2008) 5710-5723
72. Lee S., Tanaka T., Anzai K., Kirino Y., Aoyagi H., and Sugihara G. Two mode ion channels induced by interaction of acidic amphipathic alpha-helical peptides with lipid bilayers. Biochim Biophys Acta 1191 (1994) 181-189
73. Lee S.J., Chae C., and Wang M.M. p150/glued modifies nuclear estrogen receptor function. Mol Endocrinol 23 (2009) 620-629
74. Lee S.Y., Kim J.W., Jeong M.H., An J.H., Jang S.M., Song K.H., et al. Microtubule-associated protein 1B light chain (MAP1B-LC1) negatively regulates the activity of tumor suppressor p53 in neuroblastoma cells. FEBS Lett 582 (2008) 2826-2832
75. Li R., and Botchan M.R. The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein-a and stimulate in vitro BPV-1 DNA-replication. Cell 73 (1993) 1207-1221
76. Liu C.J. The role of ADAMTS-7 and Adamts-12 in the pathogenesis of arthritis. Nat Clin Pract Rheumatol 5 (2009) 38-45
77. Liu C.J., Kong W., Xu K., Luan Y., Ilalov K., Sehgal B., et al. ADAMTS-12 associates with and degrades cartilage oligomeric matrix protein. J Biol Chem 281 (2006) 15800-15808
78. Liu J., and Jiang G. CD44 and hematologic malignancies. Cell Mol Immunol 3 (2006) 359-365
79. Luan Y., Kong L., Howell D.R., Ilalov K., Fajardo M., Bai X.H., et al. Inhibition of Adamts-7 and Adamts-12 degradation of cartilage oligomeric matrix protein by alpha-2-macroglobulin. Osteoarthritis Cartilage 16 (2008) 1413-1420
80. Ma J., and Ptashne M. A new class of yeast transcriptional activators. Cell 51 (1987) 113-119
81. Makeyev E.V., Zhang J., Carrasco M.A., and Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27 (2007) 435-448
82. Nie Z., Ning W., Amagai M., and Hashimoto T. C-Terminus of desmoyokin/AHNAK protein is responsible for its translocation between the nucleus and cytoplasm. J Invest Dermatol 114 (2000) 1044-1049
83. Nilsson S.K., Haylock D.N., Johnston H.M., Occhiodoro T., Brown T.J., and Simmons P.J. Hyaluronan is synthesized by primitive hemopoietic cells, participates in their lodgment at the endosteum following transplantation, and is involved in the regulation of their proliferation and differentiation in vitro. Blood 101 (2003) 856-862
84. Nilsson S.K., Johnston H.M., Whitty G.A., Williams B., Webb R.J., Denhardt D.T., et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 106 (2005) 1232-1239
85. Noguchi C.T., Wang L., Rogers H.M., Teng R., and Jia Y. Survival and proliferative roles of erythropoietin beyond the erythroid lineage. Expert Rev Mol Med 10 (2008) e36
86. Pagourelias E.D., Koumaras C., Kakafika A.I., Tziomalos K., Zorou P.G., Athyros V.G., et al. Cardiorenal anemia syndrome: do erythropoietin and iron therapy have a place in the treatment of heart failure?. Angiology 60 (2009) 74-81
87. Pedrotti B., and Islam K. Microtubule associated protein 1B (MAP1B) promotes efficient tubulin polymerisation in vitro. FEBS Lett 371 (1995) 29-31
88. Ponta H., Sherman L., and Herrlich P.A. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4 (2003) 33-45
89. Ponti D., Costa A., Zaffaroni N., Pratesi G., Petrangolini G., Coradini D., et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65 (2005) 5506-5511
90. Ptashne M. How eukaryotic transcriptional activators work. Nature 335 (1988) 683-689
91. Richter R., Schulz-Knappe P., Schrader M., Standker L., Jurgens M., Tammen H., et al. Composition of the peptide fraction in human blood plasma: database of circulating human peptides. J Chromatogr B: Biomed Sci Appl 726 (1999) 25-35
92. Ross J.L., Wallace K., Shuman H., Goldman Y.E., and Holzbaur E.L. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat Cell Biol 8 (2006) 562-570
93. Sackstein R., Merzaban J.S., Cain D.W., Dagia N.M., Spencer J.A., Lin C.P., et al. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14 (2008) 181-187
94. Sadvakassova G., Dobocan M., and Congote L.F. Osteopontin and the C-terminal peptide of thrombospondin-4 compete for CD44 binding and have opposite effects in CD133+ cell colony formation. BMC Res Notes 2 (2009) 215
95. Sadvakassova G., Dobocan M., DiFalco M.R., and Congote L.F. Regulator of Differentiation 1 (ROD1) binds to the amphipathic C-terminal peptide of thrombospondin-4 and is involved in its mitogenic activity. J Cell Physiol 220 (2009) 672-679
96. Saha S., Ansari A.Z., Jarrell K.A., and Ptashne M. RNA sequences that work as transcriptional activating regions. Nucleic Acids Res 31 (2003) 1565-1570
97. Sawicka K., Bushell M., Spriggs K.A., and Willis A.E. Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans 36 (2008) 641-647
98. Schmits R., Filmus J., Gerwin N., Senaldi G., Kiefer F., Kundig T., et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood 90 (1997) 2217-2233
99. Screaton G.R., Bell M.V., Jackson D.G., Cornelis F.B., Gerth U., and Bell J.I. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci USA 89 (1992) 12160-12164
100. Sekiya F., Bae Y.S., Jhon D.Y., Hwang S.C., and Rhee S.G. AHNAK, a protein that binds and activates phospholipase C-gamma1 in the presence of arachidonic acid. J Biol Chem 274 (1999) 13900-13907
101. Shao Y., Czymmek K.J., Jones P.A., Fomin V.P., Akanbi K., Duncan R.L., et al. Dynamic interactions between L-type voltage sensitive calcium channel Cav1. 2 ({alpha}1C) subunits and AHNAK in osteoblastic cells. Am J Physiol Cell Physiol 296 (2009) C1067-C1078
102. Shinohara M.L., Kim H.J., Kim J.H., Garcia V.A., and Cantor H. Alternative translation of osteopontin generates intracellular and secreted isoforms that mediate distinct biological activities in dendritic cells. Proc Natl Acad Sci USA 105 (2008) 7235-7239
103. Shrum C.K., Defrancisco D., and Meffert M.K. Stimulated nuclear translocation of NF-kappaB and shuttling differentially depend on dynein and the dynactin complex. Proc Natl Acad Sci USA 106 (2009) 2647-2652
104. Shtivelman E., and Bishop J.M. Expression of CD44 is repressed in neuroblastoma cells. Mol Cell Biol 11 (1991) 5446-5453
105. Shtivelman E., and Bishop J.M. The human gene AHNAK encodes a large phosphoprotein located primarily in the nucleus. J Cell Biol 120 (1993) 625-630
106. Shtivelman E., Cohen F.E., and Bishop J.M. A human gene (AHNAK) encoding an unusually large protein with a 1.2-microns polyionic rod structure. Proc Natl Acad Sci USA 89 (1992) 5472-5476
107. Sigler P.B. Transcriptional activation. Acid blobs and negative noodles. Nature 333 (1998) 210-212
108. Smythe M.L., Huston S.E., and Marshall G.R. The molten helix-effects of solvation on the alpha-helical to 3(10)-helical transition. J Am Chem Soc 117 (1995) 5445-5452
109. Speziale M.V., and Detwiler T.C. Free thiols of platelet thrombospondin. Evidence for disulfide isomerization. J Biol Chem 265 (1990) 17859-17867
110. Stenina O.I., Desai S.Y., Krukovets I., Kight K., Janigro D., Topol E.J., et al. Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation 108 (2003) 1514-1519
111. Stier S., Ko Y., Forkert R., Lutz C., Neuhaus T., Grunewald E., et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 201 (2005) 1781-1791
112. Stiff T., Shtivelman E., Jeggo P., and Kysela B. AHNAK interacts with the DNA ligase IV-XRCC4 complex and stimulates DNA ligase IV-mediated double-stranded ligation. DNA Repair (Amst) 3 (2004) 245-256
113. Sun X., Skorstengaard K., and Mosher D.F. Disulfides modulate RGD-inhibitable cell adhesive activity of thrombospondin. J Cell Biol 118 (1992) 693-701
114. Sussman J., Stokoe D., Ossina N., and Shtivelman E. Protein kinase B phosphorylates AHNAK and regulates its subcellular localization. J Cell Biol 154 (2001) 1019-1030
115. Suzuki K., Zhu B., Rittling S.R., Denhardt D.T., Goldberg H.A., McCulloch C.A., et al. Colocalization of intracellular osteopontin with CD44 is associated with migration, cell fusion, and resorption in osteoclasts. J Bone Miner Res 17 (2002) 1486-1497
116. Taraboletti G., Morbidelli L., Donnini S., Parenti A., Granger H.J., Giavazzi R., et al. The heparin binding 25 kDa fragment of thrombospondin-1 promotes angiogenesis and modulates gelatinase and TIMP-2 production in endothelial cells. FASEB J 14 (2000) 1674-1676
117. Tortorella M., Pratta M., Liu R.Q., Abbaszade I., Ross H., Burn T., et al. The thrombospondin motif of aggrecanase-1 (ADAMTS-4) is critical for aggrecan substrate recognition and cleavage. J Biol Chem 275 (2000) 25791-25797
118. Tossi A., Sandri L., and Giangaspero A. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55 (2000) 4-30
119. Van Driel M., Gunthert U., van Kessel A.C., Joling P., Stauder R., Lokhorst H.M., et al. CD44 variant isoforms are involved in plasma cell adhesion to bone marrow stromal cells. Leukemia 16 (2002) 135-143
120. Wang K.X., and Denhardt D.T. Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev 19 (2008) 333-345
121. Wong J.M., Ionescu D., and Ingles C.J. Interaction between BRCA2 and replication protein A is compromised by a cancer-predisposing mutation in BRCA2. Oncogene 22 (2003) 28-33
122. Woodward W.A., and Sulman E.P. Cancer stem cells: markers or biomarkers?. Cancer Metastasis Rev 27 (2008) 459-470
123. Xiao H., Pearson A., Coulombe B., Truant R., Zhang S., Regier J.L., et al. Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol Cell Biol 14 (1994) 7013-7024
124. Xie Y., Yin T., Wiegraebe W., He X.C., Miller D., Stark D., et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457 (2009) 97-101
125. Yamamoto H., Tsukahara K., Kanaoka Y., Jinno S., and Okayama H. Isolation of a mammalian homologue of a fission yeast differentiation regulator. Mol Cell Biol 19 (1999) 3829-3841
126. Yamauchi E., Titani K., and Taniguchi H. Specific binding of acidic phospholipids to microtubule-associated protein MAP1B regulates its interaction with tubulin. J Biol Chem 272 (1997) 22948-22953
127. Yin T., and Li L. The stem cell niches in bone. J Clin Invest 116 (2006) 1195-1201
128. Yuryev A., Patturajan M., Litingtung Y., Joshi R.V., Gentile C., Gebara M., et al. The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc Natl Acad Sci USA 93 (1996) 6975-6980
129. Zhang J.W., and Li L.H. Stem cell niche: microenvironment and beyond. J Biol Chem 283 (2008) 9499-9503
130. Zohar R., Suzuki N., Suzuki K., Arora P., Glogauer M., McCulloch C.A., et al. Intracellular osteopontin is an integral component of the CD44-ERM complex involved in cell migration. J Cell Physiol 184 (2000) 118-130