A unique carboxyl-Terminal insert domain in the hematopoietic-Specific, gtpase-Deficient rho gtpase rhoh regulates post-Translational processing

Journal of Biological Chemistry

Volumn 288, Issue 51, 2013, Pages 36451-36462

  Troeger, Anja ^a   Chae, Hee Don ^b   Senturk, Mumine ^c   Wood, Jenna ^d   Williams, David A ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B-CELL LYMPHOMA; CARBOXYL-TERMINAL; CELL DEVELOPMENT; CHAPERONE-MEDIATED AUTOPHAGY; POST-TRANSLATIONAL PROCESSING; PROTEIN FUNCTIONS; PROTEIN LEVEL; PROTEIN STABILITY;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

CHAPERONE; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE ZAP 70; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOH PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; IN VIVO STUDY; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PRENYLATION; PROTEIN STABILITY; T LYMPHOCYTE;

ATYPICAL RHO GTPASES; AUTOPHAGY; B-CELL MALIGNANCIES; CARBOXYL TERMINUS; CHAPERONE-MEDIATED AUTOPHAGY; PROTEIN DEGRADATION; PROTEIN STABILITY; RHO GTPASES; RHOH; T CELL;

AMINO ACID MOTIFS; ANIMALS; BONE MARROW CELLS; CELL MEMBRANE; CYTOPLASM; HUMANS; JURKAT CELLS; LYSOSOMES; MICE; MICE, INBRED C57BL; MUTATION; PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; RHO GTP-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84890943716     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505727     Document Type: Article

References (57)

1. Bishop, A. L., and Hall, A. (2000) Rho GTPases and their effector proteins. Biochem. J. 348, 241-255
2. Etienne-Manneville, S., and Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635
3. Boulter, E., Garcia-Mata, R., Guilluy, C., Dubash, A., Rossi, G., Brennwald, P. J., and Burridge, K. (2010) Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat. Cell Biol. 12, 477-483
4. Dallery-Prudhomme, E., Roumier, C., Denis, C., Preudhomme, C., Kerckaert, J. P., and Galiegue-Zouitina, S. (1997) Genomic structure and assignment of the RhoH/TTF small GTPase gene (ARHH) to 4p13 by in situ hybridization. Genomics 43, 89-94
5. Preudhomme, C., Roumier, C., Hildebrand, M. P., Dallery-Prudhomme, E., Lantoine, D., Laï, J. L., Daudignon, A., Adenis, C., Bauters, F., Fenaux, P., Kerckaert, J. P., and Galiègue-Zouitina, S. (2000) Nonrandom 4p13 rearrangements of the RhoH/TTF gene, encoding a GTP-binding protein, in non-Hodgkin's lymphoma and multiple myeloma. Oncogene 19, 2023-2032
6. Pasqualucci, L., Neumeister, P., Goossens, T., Nanjangud, G., Chaganti, R. S., Küppers, R., and Dalla-Favera, R. (2001) Hypermutation of multiple protooncogenes in B-cell diffuse large-cell lymphomas. Nature 412, 341-346
7. Lahousse, S., Smorowski, A. L., Denis, C., Lantoine, D., Kerckaert, J. P., and Galiègue-Zouitina, S. (2004) Structural features of hematopoiesis-specific RhoH/ARHH gene. High diversity of 5′-UTR in different hematopoietic lineages suggests a complex post-transcriptional regulation. Gene 343, 55-68
8. Gu, Y., Chae, H. D., Siefring, J. E., Jasti, A. J., Hildeman, D. A., and Williams, D. A. (2006) RhoH GTPase recruits and activates Zap70 required for T cell receptor signaling and thymocyte development. Nat. Immunol. 7, 1182-1190
9. Dorn, T., Kuhn, U., Bungartz, G., Stiller, S., Bauer, M., Ellwart, J., Peters, T., Scharffetter-Kochanek, K., Semmrich, M., Laschinger, M., Holzmann, B., Klinkert, W. E., Straten, P. T., Køllgaard, T., Sixt, M., and Brakebusch, C. (2007) RhoH is important for positive thymocyte selection and T-cell receptor signaling. Blood 109, 2346-2355
10. Chae, H. D., Siefring, J. E., Hildeman, D. A., Gu, Y., and Williams, D. A. (2010) RhoH regulates subcellular localization of ZAP-70 and Lck in T cell receptor signaling. PloS One 5, e13970
11. Wang, H., Zeng, X., Fan, Z., and Lim, B. (2011) RhoH modulates pre-TCR and TCR signalling by regulating LCK. Cell. Signal. 23, 249-258
12. Sanchez-Aguilera, A., Rattmann, I., Drew, D. Z., Müller, L. U., Summey, V., Lucas, D. M., Byrd, J. C., Croce, C. M., Gu, Y., Cancelas, J. A., Johnston, P., Moritz, T., and Williams, D. A. (2010) Involvement of RhoH GTPase in the development of B-cell chronic lymphocytic leukemia. Leukemia 24, 97-104
13. Troeger, A., Johnson, A. J., Wood, J., Blum, W. G., Andritsos, L. A., Byrd, J. C., and Williams, D. A. (2012) RhoH is critical for cell-microenvironment interactions in chronic lymphocytic leukemia in mice and humans. Blood 119, 4708-4718
14. Gaidano, G., Pasqualucci, L., Capello, D., Berra, E., Deambrogi, C., Rossi, D., Maria Larocca, L., Gloghini, A., Carbone, A., and Dalla-Favera, R. (2003) Aberrant somatic hypermutation in multiple subtypes of AIDSassociated non-Hodgkin lymphoma. Blood 102, 1833-1841
15. Montesinos-Rongen, M., Van Roost, D., Schaller, C., Wiestler, O. D., and Deckert, M. (2004) Primary diffuse large B-cell lymphomas of the central nervous system are targeted by aberrant somatic hypermutation. Blood 103, 1869-1875
16. Crul, M., de Klerk, G. J., Beijnen, J. H., and Schellens, J. H. (2001) Ras biochemistry and farnesyl transferase inhibitors. A literature survey. Anticancer Drugs 12, 163-184
17. Li, X., Bu, X., Lu, B., Avraham, H., Flavell, R. A., and Lim, B. (2002) The hematopoiesis-specific GTP-binding protein RhoH is GTPase deficient and modulates activities of other Rho GTPases by an inhibitory function. Mol. Cell. Biol. 22, 1158-1171
18. Fueller, F., and Kubatzky, K. F. (2008) The small GTPase RhoH is an atypical regulator of haematopoietic cells. Cell Commun. Signal. 6, 6-6
19. Suwa, H., Ohshio, G., Imamura, T., Watanabe, G., Arii, S., Imamura, M., Narumiya, S., Hiai, H., and Fukumoto, M. (1998) Overexpression of the rhoC gene correlates with progression of ductal adenocarcinoma of the pancreas. Br. J. Cancer 77, 147-152
20. Adnane, J., Muro-Cacho, C., Mathews, L., Sebti, S. M., and Muñoz-Antonia, T. (2002) Suppression of rho B expression in invasive carcinoma from head and neck cancer patients. Clin. Cancer Res. 8, 2225-2232
21. Kleer, C. G., van Golen, K. L., Zhang, Y., Wu, Z. F., Rubin, M. A., and Merajver, S. D. (2002) Characterization of RhoC expression in benign and malignant breast disease. A potential new marker for small breast carcinomas with metastatic ability. Am. J. Pathol. 160, 579-584
22. Galiègue-Zouitina, S., Delestré, L., Dupont, C., Troussard, X., and Shelley, C. S. (2008) Underexpression of RhoH in hairy cell leukemia. Cancer Res. 68, 4531-4540
23. Iwasaki, T., Katsumi, A., Kiyoi, H., Tanizaki, R., Ishikawa, Y., Ozeki, K., Kobayashi, M., Abe, A., Matsushita, T., Watanabe, T., Amano, M., Kojima, T., Kaibuchi, K., and Naoe, T. (2008) Prognostic implication and biological roles of RhoH in acute myeloid leukaemia. Eur. J. Haematol. 81, 454-460
24. Delestré, L., Berthon, C., Quesnel, B., Figeac, M., Kerckaert, J. P., Galiègue-Zouitina, S., and Shelley, C. S. (2011) Repression of the RHOH gene by JunD. Biochem. J. 437, 75-88
25. Chang, X.-B., and Stewart, A. K. (2011) What is the functional role of the thalidomide binding protein cereblon? Int. J. Biochem. Mol. Biol. 2, 287-294
26. Bichi, R., Shinton, S. A., Martin, E. S., Koval, A., Calin, G. A., Cesari, R., Russo, G., Hardy, R. R., and Croce, C. M. (2002) Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc. Natl. Acad. Sci. U.S.A. 99, 6955-6960
27. Gu, Y., Jasti, A. C., Jansen, M., and Siefring, J. E. (2005) RhoH, a hematopoietic- specific Rho GTPase, regulates proliferation, survival, migration, and engraftment of hematopoietic progenitor cells. Blood 105, 1467-1475
28. Neckers, L. (2002) Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med. 8, S55-S61
29. Whitesell, L., Mimnaugh, E. G., De Costa, B., Myers, C. E., and Neckers, L. M. (1994) Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins. Essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. U.S.A. 91, 8324-8328
30. Ochel, H. J., Eichhorn, K., and Gademann, G. (2001) Geldanamycin. The prototype of a class of antitumor drugs targeting the heat shock protein 90 family of molecular chaperones. Cell Stress Chaperones 6, 105-112
31. Blagosklonny, M. V., An, W. G., Melillo, G., Nguyen, P., Trepel, J. B., and Neckers, L. M. (1999) Regulation of BRCA1 by protein degradation. Oncogene 18, 6460-6468
32. Pérez-Sala, D., Boya, P., Ramos, I., Herrera, M., and Stamatakis, K. (2009) The C-terminal sequence of RhoB directs protein degradation through an endo-lysosomal pathway. PloS One 4, e8117
33. Chae, H. D., Lee, K. E., Williams, D. A., and Gu, Y. (2008) Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood 111, 2597-2605
34. Wahlers, A., Schwieger, M., Li, Z., Meier-Tackmann, D., Lindemann, C., Eckert, H. G., von Laer, D., and Baum, C. (2001) Influence of multiplicity of infection and protein stability on retroviral vector-mediated gene expression in hematopoietic cells. Gene Ther. 8, 477-486
35. Gallardo, H. F., Tan, C., Ory, D., and Sadelain, M. (1997) Recombinant retroviruses pseudotyped with the vesicular stomatitis virus G glycoprotein mediate both stable gene transfer and pseudotransduction in human peripheral blood lymphocytes. Blood 90, 952-957
36. Viana, R., Aguado, C., Esteban, I., Moreno, D., Viollet, B., Knecht, E., and Sanz, P. (2008) Role of AMP-Activated protein kinase in autophagy and proteasome function. Biochem. Biophys. Res. Commun. 369, 964-968
37. Zungu, M., Schisler, J. C., Essop, M. F., McCudden, C., Patterson, C., and Willis, M. S. (2011) Regulation of AMPK by the ubiquitin proteasome system. Am. J. Pathol. 178, 4-11
38. Jadhav, T., and Wooten, M. W. (2009) Defining an embedded code for protein ubiquitination. J. Proteomics Bioinfor. 2, 316
39. Aguilar, R. C., and Wendland, B. (2003) Ubiquitin. Not just for proteasomes anymore. Curr. Opin. Cell Biol. 15, 184-190
40. d'Azzo, A., Bongiovanni, A., and Nastasi, T. (2005) E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 6, 429-441
41. Kraft, C., Peter, M., and Hofmann, K. (2010) Selective autophagy. Ubiquitin- mediated recognition and beyond. Nat. Cell Biol. 12, 836-841
42. Orenstein, S. J., and Cuervo, A. M. (2010) Chaperone-mediated autophagy. Molecular mechanisms and physiological relevance. Semin. Cell Dev. Biol. 21, 719-726
43. Li, W., Yang, Q., and Mao, Z. (2011) Chaperone-mediated autophagy. Machinery, regulation and biological consequences. Cell Mol. Life Sci. 68, 749-763
44. + hematopoietic cells. Hum. Gene Ther. 8, 2193-2206
45. Crequer, A., Troeger, A., Patin, E., Ma, C. S., Picard, C., Pedergnana, V., Fieschi, C., Lim, A., Abhyankar, A., Gineau, L., Mueller-Fleckenstein, I., Schmidt, M., Taieb, A., Krueger, J., Abel, L., Tangye, S. G., Orth, G., Williams, D. A., Casanova, J. L., and Jouanguy, E. (2012) Human RHOH deficiency causes T cell defects and susceptibility to EV-HPV infections. J. Clin. Investig. 122, 3239-3247
46. Sadowski, M., and Sarcevic, B. (2010) Mechanisms of mono- And polyubiquitination. Ubiquitination specificity depends on compatibility between the E2 catalytic core and amino acid residues proximal to the lysine. Cell Division 5, 19
47. van Wijk, S. J., and Timmers, H. T. (2010) The family of ubiquitin-conjugating enzymes (E2s). Deciding between life and death of proteins. FASEB J. 24, 981-993
48. Schmidt-Mende, J., Geering, B., Yousefi, S., and Simon, H. U. (2010) Lysosomal degradation of RhoH protein upon antigen receptor activation in T but not B cells. Eur. J. Immunol. 40, 525-529
49. Matsumoto, M., Oyamada, K., Takahashi, H., Sato, T., Hatakeyama, S., and Nakayama, K. I. (2009) Large-scale proteomic analysis of tyrosinephosphorylation induced by T-cell receptor or B-cell receptor activation reveals new signaling pathways. Proteomics 9, 3549-3563
50. Aspenström, P., Ruusala, A., and Pacholsky, D. (2007) Taking Rho GTPases to the next level. The cellular functions of atypical Rho GTPases. Exp. Cell Res. 313, 3673-3679
51. Gu, Y., Zheng, Y., and Williams, D. A. (2005)RhoH GTPase. A key regulator of hematopoietic cell proliferation and apoptosis? Cell Cycle 4, 201-202
52. Hiraga, J., Katsumi, A., Iwasaki, T., Abe, A., Kiyoi, H., Matsushita, T., Kinoshita, T., and Naoe, T. (2007) Prognostic analysis of aberrant somatic hypermutation of RhoH gene in diffuse large B cell lymphoma. Leukemia 21, 1846-1847
53. Su, L., Lineberry, N., Huh, Y., Soares, L., and Fathman, C. G. (2006)Anovel E3 ubiquitin ligase substrate screen identifies Rho guanine dissociation inhibitor as a substrate of gene related to anergy in lymphocytes. J. Immunol. 177, 7559-7566
54. Ryhänen, T., Hyttinen, J. M., Kopitz, J., Rilla, K., Kuusisto, E., Mannermaa, E., Viiri, J., Holmberg, C. I., Immonen, I., Meri, S., Parkkinen, J., Eskelinen, E. L., Uusitalo, H., Salminen, A., and Kaarniranta, K. (2009) Crosstalk between Hsp70 molecular chaperone, lysosomes and proteasomes in autophagy-mediated proteolysis in human retinal pigment epithelial cells. J. Cell Mol. Med. 13, 3616-3631
55. Qing, G., Yan, P., and Xiao, G. (2006) Hsp90 inhibition results in autophagy- mediated proteasome-independent degradation of IκB kinase (IKK). Cell Res. 16, 895-901
56. Qiao, L., and Zhang, J. (2009) Inhibition of lysosomal functions reduces proteasomal activity. Neurosci. Lett. 456, 15-19
57. Benbrook, D. M., and Long, A. (2012) Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp. Oncol. 34, 286-297