Deficiency of GRP94 in the hematopoietic system alters proliferation regulators in hematopoietic stem cells

Stem Cells and Development

Volumn 22, Issue 23, 2013, Pages 3062-3073

  Luo, Biquan ^a   Tseng, Chun Chih ^a   Adams, Gregor B ^a   Lee, Amy S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; CELL SURFACE PROTEIN; CHEMOKINE RECEPTOR CXCR4; CONNEXIN 32; GLUCOSE REGULATED PROTEIN 94; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ARTICLE; BONE MARROW; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN CELL;

ANIMALS; ANTIGENS, LY; BONE MARROW CELLS; CELL MEMBRANE; CELL PROLIFERATION; CELLS, CULTURED; CONNEXINS; DOWN-REGULATION; ENZYME ACTIVATION; GENE DELETION; HEMATOPOIETIC STEM CELLS; HEMATOPOIETIC SYSTEM; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PEPTIDES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, TIE-2; RECEPTORS, CXCR4;

EID: 84888612260     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0181     Document Type: Article

References (56)

1. Zon LI. (2008). Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453:306-313.
2. Orford KW and DT Scadden. (2008). Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115-128.
3. Kharas MG and K Gritsman. (2010). Akt: a double-edged sword for hematopoietic stem cells. Cell Cycle 9:1223-1224.
4. Yilmaz OH, R Valdez, BK Theisen, W Guo, DO Ferguson, H Wu and SJ Morrison. (2006). Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441:475-482.
5. Zhang J, JC Grindley, T Yin, S Jayasinghe, XC He, JT Ross, JS Haug, D Rupp, KS Porter-Westpfahl, et al. (2006). PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441:518-522.
6. Kharas MG, R Okabe, JJ Ganis, M Gozo, T Khandan, M Paktinat, DG Gilliland and K Gritsman. (2010). Constitutively active AKT depletes hematopoietic stem cells and induces leukemia in mice. Blood 115:1406-1415.
7. Pietras EM, MR Warr and E Passegue. (2011). Cell cycle regulation in hematopoietic stem cells. J Cell Biol 195: 709-720.
8. Donato JL, J Ko, JL Kutok, T Cheng, T Shirakawa, XQ Mao, D Beach, DT Scadden, MH Sayegh and CN Adra. (2002). Human HTm4 is a hematopoietic cell cycle regulator. J Clin Invest 109:51-58.
9. Kutok JL, X Yang, R Folkerth and CN Adra. (2011). Characterization of the expression of HTm4 (MS4A3), a cell cycle regulator, in human peripheral blood cells and normal and malignant tissues. J Cell Mol Med 15:86-93.
10. Chinami M, Y Yano, X Yang, S Salahuddin, K Moriyama, M Shiroishi, H Turner, T Shirakawa and CN Adra. (2005). Binding of HTm4 to cyclin-dependent kinase (Cdk)- associated phosphatase (KAP).Cdk2.cyclin A complex enhances the phosphatase activity of KAP, dissociates cyclin A, and facilitates KAP dephosphorylation of Cdk2. J Biol Chem 280:17235-17242.
11. Wilson A and A Trumpp. (2006). Bone-marrow haematopoietic- stem-cell niches. Nat Rev Immunol 6:93-106.
12. Jones DL and AJ Wagers. (2008). No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9:11-21.
13. Cheng T. (2008). Toward 'SMART' stem cells. Gene Ther 15:67-73.
14. Kiel MJ, OH Yilmaz, T Iwashita, C Terhorst and SJ Morrison. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109-1121.
15. Mendez-Ferrer S, TV Michurina, F Ferraro, AR Mazloom, BD Macarthur, SA Lira, DT Scadden, A Ma'ayan, GN Enikolopov and PS Frenette. (2010). Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829-834.
16. Ding L, TL Saunders, G Enikolopov and SJ Morrison. (2012). Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457-462.
17. Greenbaum A, YM Hsu, RB Day, LG Schuettpelz, MJ Christopher, JN Borgerding, T Nagasawa and DC Link. (2013). CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495:227-230.
18. Nie Y, YC Han and YR Zou. (2008). CXCR4 is required for the quiescence of primitive hematopoietic cells. J Exp Med 205:777-783.
19. Arai F, A Hirao, M Ohmura, H Sato, S Matsuoka, K Takubo, K Ito, GY Koh and T Suda. (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118:149-161.
20. Adams GB, KT Chabner, IR Alley, DP Olson, ZM Szczepiorkowski, MC Poznansky, CH Kos, MR Pollak, EM Brown and DT Scadden. (2006). Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 439:599-603.
21. Taichman RS. (2005). Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105:2631-2639.
22. Mendez-Ferrer S and PS Frenette. (2007). Hematopoietic stem cell trafficking: regulated adhesion and attraction to bone marrow microenvironment. Ann N Y Acad Sci 1116: 392-413.
23. Priestley GV, LM Scott, T Ulyanova and T Papayannopoulou. (2006). Lack of alpha4 integrin expression in stem cells restricts competitive function and self-renewal activity. Blood 107:2959-2967.
24. Forsberg EC and S Smith-Berdan. (2009). Parsing the niche code: the molecular mechanisms governing hematopoietic stem cell adhesion and differentiation. Haematologica 94: 1477-1481.
25. Gonzalez-Nieto D, L Li, A Kohler, G Ghiaur, E Ishikawa, A Sengupta, M Madhu, JL Arnett, RA Santho, et al. (2012). Connexin-43 in the osteogenic BM niche regulates its cellular composition and the bidirectional traffic of hematopoietic stem cells and progenitors. Blood 119:5144-5154.
26. Hirabayashi Y, BI Yoon, I Tsuboi, Y Huo, Y Kodama, J Kanno, T Ott, JE Trosko and T Inoue. (2007). Membrane channel connexin 32 maintains Lin( - )/c-kit( + ) hematopoietic progenitor cell compartment: analysis of the cell cycle. J Membr Biol 217:105-113.
27. Ni M and AS Lee. (2007). ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641-3651.
28. Marzec M, D Eletto and Y Argon. (2012). GRP94: an HSP90- like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochim Biophys Acta 1823:774-787.
29. Liu B, M Staron, F Hong, BX Wu, S Sun, C Morales, CE Crosson, S Tomlinson, I Kim, D Wu and Z Li. (2013). Essential roles of grp94 in gut homeostasis via chaperoning canonical Wnt pathway. Proc Natl Acad Sci U S A 110:6877-6882.
30. Luo B, BS Lam, SH Lee, S Wey, H Zhou, M Wang, SY Chen, GB Adams and AS Lee. (2011). The endoplasmic reticulum chaperone protein GRP94 is required for maintaining hematopoietic stem cell interactions with the adult bone marrow niche. PLoS One 6:e20364.
31. Hirai H, H Sootome, Y Nakatsuru, K Miyama, S Taguchi, K Tsujioka, Y Ueno, H Hatch, PK Majumder, BS Pan and H Kotani. (2010). MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol Cancer Ther 9:1956-1967.
32. Maezawa I and LW Jin. (2010). Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30:5346-5356.
33. Wang N, M De Bock, G Antoons, AK Gadicherla, M Bol, E Decrock, WH Evans, KR Sipido, FF Bukauskas and L Leybaert. (2012). Connexin mimetic peptides inhibit Cx43 hemichannel opening triggered by voltage and intracellular Ca2 + elevation. Basic Res Cardiol 107:304.
34. el-Fouly MH, JE Trosko and CC Chang. (1987). Scrapeloading and dye transfer. A rapid and simple technique to study gap junctional intercellular communication. Exp Cell Res 168:422-430.
35. Plantard L, M Huber, F Macari, P Meda and D Hohl. (2003). Molecular interaction of connexin 30.3 and connexin 31 suggests a dominant-negative mechanism associated with erythrokeratodermia variabilis. Hum Mol Genet 12:3287-3294.
36. Wey S, B Luo, CC Tseng, M Ni, H Zhou, Y Fu, D Bhojwani, WL Carroll and AS Lee. (2012). Inducible knockout of GRP78/BiP in the hematopoietic system suppresses Ptennull leukemogenesis and AKT oncogenic signaling. Blood 119:817-825.
37. Gray MJ, P Mhawech-Fauceglia, E Yoo, W Yang, E Wu, AS Lee and YG Lin. (2013). AKT inhibition mitigates GRP78 (glucose-regulated protein) expression and contribution to chemoresistance in endometrial cancers. Int J Cancer 133:21-30.
38. De Vuyst E, E Decrock, L Cabooter, GR Dubyak, CC Naus, WH Evans and L Leybaert. (2006). Intracellular calcium changes trigger connexin 32 hemichannel opening. EMBO J 25:34-44.
39. Takeuchi H, S Jin, J Wang, G Zhang, J Kawanokuchi, R Kuno, Y Sonobe, T Mizuno and A Suzumura. (2006). Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281:21362-21368.
40. Ding L and SJ Morrison. (2013). Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495:231-235.
41. Smith-Berdan S, A Nguyen, D Hassanein, M Zimmer, F Ugarte, J Ciriza, D Li, ME Garcia-Ojeda, L Hinck and EC Forsberg. (2011). Robo4 cooperates with CXCR4 to specify hematopoietic stem cell localization to bone marrow niches. Cell Stem Cell 8:72-83.
42. Liu B and Z Li. (2008). Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin. Blood 112:1223-1230.
43. Maynard JC, T Pham, T Zheng, A Jockheck-Clark, HB Rankin, CB Newgard, EP Spana and CV Nicchitta. (2010). Gp93, the Drosophila GRP94 ortholog, is required for gut epithelial homeostasis and nutrient assimilation-coupled growth control. Dev Biol 339:295-306.
44. Kaplan IM, S Morisot, D Heiser, WC Cheng, MJ Kim and CI Civin. (2011). Deletion of tristetraprolin caused spontaneous reactive granulopoiesis by a non-cell-autonomous mechanism without disturbing long-term hematopoietic stem cell quiescence. J Immunol 186:2826-2834.
45. Staron M, Y Yang, B Liu, J Li, Y Shen, JC Zuniga-Pflucker, HL Aguila, I Goldschneider and Z Li. (2010). gp96, an endoplasmic reticulum master chaperone for integrins and Toll-like receptors, selectively regulates early T and B lymphopoiesis. Blood 115:2380-2390.
46. Kapur R, R Cooper, L Zhang and DA Williams. (2001). Cross-talk between alpha(4)beta(1)/alpha(5)beta(1) and c- Kit results in opposing effect on growth and survival of hematopoietic cells via the activation of focal adhesion kinase, mitogen-activated protein kinase, and Akt signaling pathways. Blood 97:1975-1981.
47. Jiang Y, H Bonig, T Ulyanova, K Chang and T Papayannopoulou. (2009). On the adaptation of endosteal stem cell niche function in response to stress. Blood 114:3773-3782.
48. Rokudai S, N Fujita, Y Hashimoto and T Tsuruo. (2000). Cleavage and inactivation of antiapoptotic Akt/PKB by caspases during apoptosis. J Cell Physiol 182:290-296.
49. Mao C, M Wang, B Luo, S Wey, D Dong, R Wesselschmidt, S Rawlings and AS Lee. (2010). Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS One 5:e10852.
50. Li M, Z Zhang, DL Hill, H Wang and R Zhang. (2007). Curcumin, a dietary component, has anticancer, chemosensitization, and radiosensitization effects by down-regulating the MDM2 oncogene through the PI3K/mTOR/ETS2 pathway. Cancer Res 67:1988-1996.
51. Johnson SM, P Gulhati, I Arrieta, X Wang, T Uchida, T Gao and BM Evers. (2009). Curcumin inhibits proliferation of colorectal carcinoma by modulating Akt/mTOR signaling. Anticancer Res 29:3185-3190.
52. Fu Y, S Wey, M Wang, R Ye, CP Liao, P Roy-Burman and AS Lee. (2008). Pten null prostate tumorigenesis and AKT activation are blocked by targeted knockout of ER chaperone GRP78/BiP in prostate epithelium. Proc Natl Acad Sci U S A 105:19444-19449.
53. Luo B and AS Lee. (2013). The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 32:805-818.
54. Morita Y, A Iseki, S Okamura, S Suzuki, H Nakauchi and H Ema. (2011). Functional characterization of hematopoietic stem cells in the spleen. Exp Hematol 39:351-359.e353.
55. O'Neill HC. (2012). Niches for extramedullary hematopoiesis in the spleen. Niche 1:12-16.
56. Plante I, M Charbonneau and DG Cyr. (2006). Activation of the integrin-linked kinase pathway downregulates hepatic connexin32 via nuclear Akt. Carcinogenesis 27:1923-1929.