Human stanniocalcin-1 interacts with nuclear and cytoplasmic proteins and acts as a SUMO E3 ligase

Molecular BioSystems

Volumn 7, Issue 1, 2011, Pages 180-193

  Dos Santos, Marcos Tadeu ^a,b   Trindade, Daniel Maragno ^a   De Almeida Gonçalves, Kaliandra ^a,b   Bressan, Gustavo Costa ^c   Anastassopoulos, Filipe ^a   Yunes, José Andres ^d   Kobarg, Jörg ^a,b  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^d CENTRO INFANTIL BOLDRINI   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; HYPOCALCIN; NUCLEAR PROTEIN; SUMO 1 PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CLASSIFICATION; CYTOPLASM; DNA SEQUENCE; GENETICS; HUMAN; IMMUNOPRECIPITATION; METABOLISM; METHODOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN BINDING; TUMOR CELL CULTURE; TWO HYBRID SYSTEM;

CYTOPLASM; GLYCOPROTEINS; HUMANS; IMMUNOPRECIPITATION; NUCLEAR PROTEINS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SEQUENCE ANALYSIS, DNA; SUMO-1 PROTEIN; TUMOR CELLS, CULTURED; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-PROTEIN LIGASES;

EID: 78650130581     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c0mb00088d     Document Type: Article

References (88)

1. J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease Nat. Med. 1995 1 27 31
2. P. O. Iversen D. R. Sorensen H. B. Benestad Inhibitors of angiogenesis selectively reduce the malignant cell load in rodent models of human myeloid leukemias Leukemia 2002 16 376 381
3. J. P. Veiga L. F. Costa S. E. Sallan L. M. Nadler A. A. Cardoso Leukemia-stimulated bone marrow endothelium promotes leukemia cell survival Exp. Hematol. 2006 34 610 621
4. A. C. Chang J. Janosi M. Hulsbeek D. de Jong K. J. Jeffrey J. R. Noble R. R. Reddel A novel human cDNA highly homologous to the fish hormone stanniocalcin Mol. Cell. Endocrinol. 1995 112 241 247
5. A. C. Chang D. A. Jellinek R. R. Reddel Mammalian stanniocalcins and cancer Endocr. Relat. Cancer 2003 10 359 373
6. R. A. Wascher K. T. Huynh A. E. Giuliano N. M. Hansen F. R. Singer D. Elashoff D. S. Hoon Stanniocalcin-1: a novel molecular blood and bone marrow marker for human breast cancer Clin. Cancer Res. 2006 9 1427 1435
7. M. E. Gerritsen R. Soriano S. Yang G. Ingle C. Zlot K. Toy J. Winer A. Draksharapu F. Peale T. D. Wu P. M. Williams In silico data filtering to identify new angiogenesis targets from a large in vitro gene profiling data set Physiol. Genomics 2002 10 13 20
8. D. M. Anderson B. J. Beres J. Wilson-Rawls A. Rawls The homeobox gene Mohawk represses transcription by recruiting the sin3A/HDAC co-repressor complex Dev. Dyn. 2009 238 572 580
9. J. Kahn F. Mehraban G. Ingle X. Xin J. E. Bryant G. Vehar J. Schoenfeld C. J. Grimaldi F. Peale A. Draksharapu D. A. Lewin M. E. Gerritsen Gene expression profiling in an in vitro model of angiogenesis Am. J. Pathol. 2000 156 1887 1900
10. D. Liu H. Jia D. I. Holmes A. Stannard I. Zachary Vascular endothelial growth factor-regulated gene expression in endothelial cells: KDR-mediated induction of Egr3 and the related nuclear receptors Nur77, Nurr1, and Nor1 Arterioscler., Thromb., Vasc. Biol. 2003 23 2002 2007
11. K. K. Wary G. D. Thakker J. O. Humtsoe J. Yang Analysis of VEGF-responsive genes involved in the activation of endothelial cells Mol. Cancer 2003 2 25
12. D. Sheikh-Hamad Mammalian stanniocalcin-1 activates mitochondrial antioxidant pathways: new paradigms for regulation of macrophages and endothelium Am. J. Physiol.: Renal Physiol. 2010 298 F248 F254
13. C. R. Mccudden K. A. James C. Hasilo G. F. Wagner Characterization of mammalian stanniocalcin receptors. Mitochondrial targeting of ligand and receptor for regulation of cellular metabolism J. Biol. Chem. 2002 277 45249 45258
14. C. P. Hasilo C. R. Mccudden J. R. Gillespie K. A. James E. R. Hirvi D. Zaidi G. F. Wagner Nuclear targeting of stanniocalcin to mammary gland alveolar cells during pregnancy and lactation Am. J. Physiol.: Endocrinol. Metab. 2005 289 E634 E642
15. D. A. Jellinek A. C. Chang M. R. Larsen X. Wang P. J. Robinson R. R. Reddel Stanniocalcin 1 and 2 are secreted as phosphoproteins from human fibrosarcoma cells Biochem. J. 2000 350 Pt 2 453 461
16. J. Lomax Get ready to GO! A biologist's guide to the Gene Ontology Briefings Bioinf. 2005 6 298 304
17. K. Nakai P. Horton PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization Trends Biochem. Sci. 1999 24 34 36
18. D. M. Trindade J. C. Silva M. S. Navarro C. Torriani J. Kobarg Low-resolution structural studies of human Stanniocalcin-1 BMC Struct. Biol. 2009 9 57
19. K. F. Kelly J. M. Daniel POZ for effect - POZ-ZF transcription factors in cancer and development Trends Cell Biol. 2006 16 578 587
20. J. Raberger A. Schebesta S. Sakaguchi N. Boucheron K. E. Blomberg A. Berglof T. Kolbe C. I. Smith T. Rulicke W. Ellmeier The transcriptional regulator PLZF induces the development of CD44 high memory phenotype T cells Proc. Natl. Acad. Sci. U. S. A. 2008 105 17919 17924
21. Y. Xue F. Zhou C. Fu Y. Xu X. Yao SUMOsp: a web server for SUMOylation site prediction Nucleic Acids Res. 2006 34 1 W254 W257
22. M. B. Kroetz and M. Hochstrasser, SUMO protocols, Human Press, 2009, vol. 1, pp. 107-120
23. G. F. Wagner G. E. Dimattia The stanniocalcin family of proteins J. Exp. Zool. A Comp. Exp. Biol. 2006 305 9 769 780
24. G. Tremblay P. Bernier-Dodier L. Delbecchi G. F. Wagner B. G. Talbot P. Lacasse Local control of mammary involution: is stanniocalcin-1 involved? J. Dairy Sci. 2009 92 5 1998 2006
25. G. Basini L. Baioni S. Bussolati S. Grolli L. H. Kramer G. F. Wagner F. Grasselli Expression and localization of stanniocalcin 1 in swine ovary Gen. Comp. Endocrinol. 2010 166 2 404 408
26. J. Johnston Y. Ramos-Valdes L. A. Stanton S. Ladhani F. Beier G. E. Dimattia Human stanniocalcin-1 or -2 expressed in mice reduces bone size and severely inhibits cranial intramembranous bone growth Transgenic Res. 2010 10.1007/s11248-010-9376-7
27. A. Zimber Q. D. Nguyen C. Gespach Nuclear bodies and compartments: functional roles and cellular signalling in health and disease Cell. Signalling 2004 16 1085 1104
28. T. H. Shen H. K. Lin P. P. Scaglioni T. M. Yung P. P. Pandolfi The mechanisms of PML-nuclear body formation Mol. Cell 2006 3 331 339
29. Y. Zhang R. Iratni H. Erdjument-Bromage P. Tempst D. Reinberg Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex Cell 1997 89 3 357 364
30. Y. Tohmiya Y. Koide S. Fujimaki H. Harigae T. Funato M. Kaku T. Ishii Y. Munakata J. Kameoka T. Sasaki Stanniocalcin-1 as a novel marker to detect minimal residual disease of human leukemia Tohoku J. Exp. Med. 2004 204 2 125 133
31. R. I. Kumaran R. Thakar D. L. Spector Chromatin dynamics and gene positioning Cell 2008 132 929 934
32. R. I. Kumaran B. Muralikrishna V. K. Parnaik Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription J. Cell Biol. 2002 159 783 793
33. N. Sylvius Z. T. Bilinska J. P. Veinot A. Fidzianska P. M. Bolongo S. Poon P. McKeown R. A. Davies K. L. Chan A. S. Tang S. Dyack J. Grzybowski W. Ruzyllo H. McBride F. Tesson In vivo and in vitro examination of the functional significances of novel lamin gene mutations in heart failure patients J. Med. Genet. 2005 42 639 647
34. N. Sylvius A. Hathaway E. Boudreau P. Gupta S. Labib P. M. Bolongo P. Rippstein H. Mcbride Z. T. Bilinska F. Tesson Specific contribution of lamin A and lamin C in the development of laminopathies Exp. Cell Res. 2008 314 2362 2375
35. M. K. Andersson A. Stahlberg Y. Arvidsson A. Olofsson H. Semb G. Stenman O. Nilsson P. Aman The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response BMC Cell Biol. 2008 9 37
36. W. Hackl R. Luhrmann Molecular cloning and subcellular localization of the snRNP-associated protein 69 KD, a structural homologue of the proto-oncoproteins TLS and EWS with RNA and DNA-binding properties J. Mol. Biol. 1996 264 843 851
37. H. Y. Yeung K. P. Lai H. Y. Chan N. K. Mak G. F. Wagner C. K. Wong Hypoxia-inducible factor-1-mediated activation of stanniocalcin-1 in human cancer cells Endocrinology 2005 146 4951 4960
38. D. Ito J. R. Walker C. S. Thompson I. Moroz W. Lin M. L. Veselits A. M. Hakim A. A. Fienberg G. Thinakaran Characterization of stanniocalcin 2, a novel target of the mammalian unfolded protein response with cytoprotective properties Mol. Cell. Biol. 2004 24 9456 9469
39. S. M. Oh Z. Liu M. Okada W. Jang X. Liu C. B. Chan H. Luo K. Ye Ebp1 SUMOylation, regulated by TLS/FUS E3 ligase, is required for its anti-proliferative activity Oncogene 2010 29 7 1017 1030
40. M. J. Edelmann A. Iphöfer M. Akutsu M. Altun K. di Gleria H. B. Kramer E. Fiebiger S. Dhe-Paganon B. M. Kessler Structural basis and specificity of human otubain 1-mediated deubiquitination Biochem. J. 2009 418 2 379 390
41. F. C. Nery D. O. Passos V. S. Garcia J. Kobarg Ki-1/57 interacts with RACK1 and is a substrate for the phosphorylation by phorbol 12-myristate 13-acetate-activated protein kinase C J. Biol. Chem. 2004 279 12 11444 11455
42. I. Gillot C. Matthews D. Puel F. Vidal P. Lopez Ret Finger Protein: An E3 Ubiquitin Ligase Juxtaposed to the XY Body in Meiosis Int. J. Cell Biol. 2009 524858
43. J. P. Bocock S. Carmicle E. Madamba A. H. Erickson Nuclear Targeting of an Endosomal E3 Ubiquitin Ligase Traffic 2010 11 6 756 766
44. Y. Takahashi V. Lallemand-Breitenbach J. Zhu H. de The PML nuclear bodies and apoptosis Oncogene 2004 23 2819 2824
45. 3-induced PML or PML/retinoic acid receptor alpha degradation J. Exp. Med. 2001 193 1361 1371
46. P. Dhordain O. Albagli N. Honore F. Guidez D. Lantoine M. Schmid H. D. The A. Zelent M. H. Koken Colocalization and heteromerization between the two human oncogene POZ/zinc finger proteins, LAZ3 (BCL6) and PLZF Oncogene 2000 19 6240 6250
47. E. de Stanchina E. Querido M. Narita R. V. Davuluri P. P. Pandolfi G. Ferbeyre S. W. Lowe PML is a direct p53 target that modulates p53 effector functions Mol. Cell 2004 13 523 535
48. E. Krieghoff-Henning T. G. Hofmann Role of nuclear bodies in apoptosis signaling Biochim. Biophys. Acta 2008 1783 2185 2194
49. K. P. Lai A. Y. Law H. Y. Yeung L. S. Lee G. F. Wagner C. K. Wong Induction of stanniocalcin-1 expression in apoptotic human nasopharyngeal cancer cells by p53 Biochem. Biophys. Res. Commun. 2007 356 968 975
50. S. Weidtkamp-Peters T. Lenser D. Negorev N. Gerstner T. G. Hofmann G. Schwanitz C. Hoischen G. Maul P. Dittrich P. Hemmerich Dynamics of component exchange at PML nuclear bodies J. Cell Sci. 2008 121 16 2731 2743
51. E. van Damme K. Laukens T. H. Dang X. van Ostade A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics Int. J. Biol. Sci. 2010 6 1 51 67
52. S. A. McCallum J. F. Bazan M. Merchant J. Yin B. Pan F. J. de Sauvage W. J. Fairbrother Structure of SAP18: a ubiquitin fold in histone deacetylase complex assembly Biochemistry 2006 45 11974 11982
53. A. R. Daniel C. A. Lange Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 2009 106 34 14287 14292
54. C. Gao X. Cheng M. Lam Y. Liu Q. Liu K. S. Chang H. Y. Kao Signal-dependent regulation of transcription by histone deacetylase 7 involves recruitment to promyelocytic leukemia protein nuclear bodies Mol. Biol. Cell. 2008 19 3020 3027
55. C. Gao C. C. Ho E. Reineke M. Lam X. Cheng K. J. Stanya Y. Liu S. Chakraborty H. M. Shih H. Y. Kao Histone deacetylase 7 promotes PML SUMOylation and is essential for PML nuclear body formation Mol. Cell. Biol. 2008 28 5658 5667
56. K. Oh-Hashi Y. Naruse F. Amaya G. Shimosato M. Tanaka Cloning and characterization of a novel GRP78-binding protein in the rat brain J. Biol. Chem. 2003 278 10531 10537
57. J. D. Malhotra R. J. Kaufman The endoplasmic reticulum and the unfolded protein response Semin. Cell Dev. Biol. 2007 18 716 731
58. J. N. Gass H. Y. Jiang R. C. Wek J. W. Brewer The unfolded protein response of B-lymphocytes: PERK-independent development of antibody-secreting cells Mol. Immunol. 2008 45 1035 1043
59. T. Iwawaki R. Akai S. Yamanaka K. Kohno Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability Proc. Natl. Acad. Sci. U. S. A. 2009 106 39 16657 16662
60. 2+ release in skeletal muscle J. Physiol. 2006 572 269 280
61. E. Rios Calcium signalling in muscle: a milestone for modulation studies J. Physiol. 2006 572 1 2
62. H. S. Olsen M. A. Cepeda Q. Q. Zhang C. A. Rosen B. L. Vozzolo Human stanniocalcin: a possible hormonal regulator of mineral metabolism Proc. Natl. Acad. Sci. U. S. A. 1996 93 1792 1796
63. G. F. Wagner B. L. Vozzolo E. Jaworski M. Haddad R. L. Kline H. S. Olsen C. A. Rosen M. B. Davidson J. L. Renfro Human stanniocalcin inhibits renal phosphate excretion in the rat J. Bone Miner. Res. 1997 12 165 171
64. K. L. Madsen M. M. Tavernini C. Yachimec D. L. Mendrick P. J. Alfonso M. Buergin H. S. Olsen M. J. Antonaccio A. B. Thomson R. N. Fedorak Stanniocalcin: a novel protein regulating calcium and phosphate transport across mammalian intestine Am. J. Physiol. 1998 274 G96 G102
65. D. Sheikh-Hamad R. Bick G. Y. Wu B. M. Christensen P. Razeghi B. Poindexter H. Taegtmeyer A. Wamsley R. Padda M. Entman S. Nielsen K. Youker Stanniocalcin-1 is a naturally occurring L-channel inhibitor in cardiomyocytes: relevance to human heart failure Am. J. Physiol. Heart Circ. Physiol. 2003 285 H442 H448
66. D. Sheikh-Hamad D. Rouse Y. Yang Regulation of stanniocalcin in MDCK cells by hypertonicity and extracellular calcium Am. J. Physiol. Renal Physiol. 2000 278 F417 F424
67. 2+ overload and cell hypercontracture in cardiomyocytes Circ. J. 2007 71 796 801
68. J. P. Ellard C. R. McCudden C. Tanega K. A. James S. Ratkovic J. F. Staples G. F. Wagner The respiratory effects of stanniocalcin-1 (STC1) on intact mitochondria and cells: STC1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates Mol. Cell. Endocrinol. 2007 264 90 101
69. P. P. Roux J. Blenis ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions Microbiol. Mol. Biol. Rev. 2004 68 320 344
70. D. I. Holmes I. C. Zachary Vascular endothelial growth factor regulates stanniocalcin-1 expression via neuropilin-1-dependent regulation of KDR and synergism with fibroblast growth factor-2 Cell. Signalling 2008 20 569 579
71. K. James M. Seitelbach C. R. Mccudden G. F. Wagner Evidence for stanniocalcin binding activity in mammalian blood and glomerular filtrate Kidney Int. 2005 67 477 482
72. S. V. Bhagwat J. Lahdenranta R. Giordano W. Arap R. Pasqualini L. H. Shapiro CD13/APN is activated by angiogenic signals and is essential for capillary tube formation Blood 2001 97 652 659
73. R. Pasqualini E. Koivunen R. Kain J. Lahdenranta M. Sakamoto A. Stryhn R. A. Ashmun L. H. Shapiro W. Arap E. Ruoslahti Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis Cancer Res. 2000 60 722 727
74. J. Zhong Y. Wang X. Qiu X. Mo Y. Liu T. Li Q. Song D. Ma W. Han Characterization and expression profile of CMTM3/CKLFSF3 J. Biochem. Mol. Biol. 2006 39 537 545
75. Y. Wang T. Li X. Qiu X. Mo Y. Zhang Q. Song D. Ma W. Han CMTM3 can affect the transcription activity of androgen receptor and inhibit the expression level of PSA in LNCaP cells Biochem. Biophys. Res. Commun. 2008 371 54 58
76. A. Teufel N. Malik M. Mukhopadhyay H. Westphal Frcp1 and Frcp2, two novel fibronectin type III repeat containing genes Gene 2002 297 1-2 79 83
77. E. Beillard N. Pallisgaard d. V. V. Van W. Bi R. Dee S. E. van der E. Delabesse E. Macintyre E. Gottardi G. Saglio F. Watzinger T. Lion J. J. van Dongen P. Hokland J. Gabert Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program Leukemia 2003 17 2474 2486
78. F. R. Carneiro T. C. Silva A. C. Alves T. Haline-Vaz F. C. Gozzo N. I. Zanchin Spectroscopic characterization of the tumor antigen NY-REN-21 and identification of heterodimer formation with SCAND1 Biochem. Biophys. Res. Commun. 2006 343 260 268
79. E. M. Assmann M. R. Alborghetti M. E. Camargo J. Kobarg FEZ1 dimerization and interaction with transcription regulatory proteins involves its coiled-coil region J. Biol. Chem. 2006 281 9869 9881
80. M. Johnson I. Zaretskaya Y. Raytselis Y. Merezhuk S. McGinnis T. L. Madden NCBI BLAST: a better web interface Nucleic Acids Res. 2008 36 W5 W9
81. T. A. Lemos D. O. Passos F. C. Nery J. Kobarg Characterization of a new family of proteins that interact with the C-terminal region of the chromatin-remodeling factor CHD-3 FEBS Lett. 2003 533 14 20
82. J. Kobarg S. Schnittger C. Fonatsch H. Lemke M. A. Bowen F. Buck H. P. Hansen Characterization, mapping and partial cDNA sequence of the 57 kDa intracellular Ki-1 antigen Exp. Clin. Immunogenet. 1997 14 273 280
83. B. J. Breitkreutz C. Stark M. Tyers Osprey: a network visualization system Genome Biol. 2003 4 R22
84. B. J. Breitkreutz C. Stark T. Reguly L. Boucher A. Breitkreutz M. Livstone R. Oughtred D. H. Lackner J. Bahler V. Wood K. Dolinski M. Tyers The BioGRID Interaction Database: 2008 Nucleic Acids Res. 2008 36 D637 D640
85. C. Stark B. J. Breitkreutz T. Reguly L. Boucher A. Breitkreutz M. Tyers BioGRID: a general repository for interaction datasets Nucleic Acids Res. 2006 34 D535 D539
86. H. D. Ulrich, The SUMO system: an Overview, SUMO protocols, Human Press, 2009, vol. 1, pp. 3-16
87. S. H. Yang A. Galanis J. Witty A. D. Sharrocks An extended consensus motif enhances the specificity of substrate modification by SUMO EMBO J. 2006 25 5083 5093
88. D. Maglott J. Ostell K. D. Pruitt T. Tatusova Entrez Gene: gene-centered information at NCBI Nucleic Acids Res. 2007 35 D26 D31