Chromatin modifying protein 1A (Chmp1A) of the endosomal sorting complex required for transport (ESCRT)-III family activates ataxia telangiectasia mutated (ATM) for PanC-1 cell growth inhibition

Cell Cycle

Volumn 10, Issue 15, 2011, Pages 2529-2539

  Manohar, Sumanth ^b   Harlow, Matthew ^a   Nguyen, Hahn ^a   Li, Jing ^a   Hankins, Gerald R ^b   Park, Maiyon ^a  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEST VIRGINIA STATE UNIVERSITY   (United States)

Author keywords

ATM; Chmp1A; ESCRT III; p53; Pancreatic cancer

Indexed keywords

ATM PROTEIN; CHROMATIN MODIFYING PROTEIN 1A; ESCRT PROTEIN; PROTEIN P53; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL GROWTH; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA;

EID: 79961115262     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.15.15926     Document Type: Article

References (51)

1. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983; 97:329-39; PMID: 6309857; DOI: 10.1083/jcb.97.2.329.
2. Opresko LK, Chang CP, Will BH, Burke PM, Gill GN, Wiley HS. Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of the tyrosine kinase domain. J Biol Chem 1995; 270:4325-33; PMID: 7876194; DOI: 10.1074/jbc.270.9.4325.
3. Hurley JH. ESCRT complexes and the biogenesis of multivesicular bodies. Curr Opin Cell Biol 2008; 20:4-11; PMID: 18222686; DOI: 10.1016/j.ceb.2007.12. 002.
4. Piper RC, Katzmann DJ. Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 2007; 23:519-47; PMID: 17506697; DOI: 10.1146/annurev.cellbio.23.090506.123319.
5. Bouamr F, Houck-Loomis BR, De Los Santos M, Casaday RJ, Johnson MC, Goff SP. The C-terminal portion of the Hrs protein interacts with Tsg101 and interferes with human immunodeficiency virus type 1 Gag particle production. J Virol 2007; 81:2909-22; PMID: 17182674; DOI: 10.1128/JVI.01413-06.
6. Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, Emr SD, et al. Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J 2007; 26:600-12; PMID: 17215868; DOI: 10.1038/sj.emboj.7601501.
7. Kostelansky MS, Schluter C, Tam YY, Lee S, Ghirlando R, Beach B, et al. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 2007; 129:485-98; PMID: 17442384; DOI: 10.1016/j.cell.2007. 03.016.
8. Obita T, Saksena S, Ghazi-Tabatabai S, Gill DJ, Perisic O, Emr SD, et al. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 2007; 449:735-9; PMID: 17928861; DOI: 10.1038/nature06171.
9. Stuchell-Brereton MD, Skalicky JJ, Kieffer C, Karren MA, Ghaffarian S, Sundquist WI. ESCRT-III recognition by VPS4 ATPases. Nature 2007; 449:740-4; PMID: 17928862; DOI: 10.1038/nature06172.
10. Xiao J, Xia H, Yoshino-Koh K, Zhou J, Xu Z. Structural characterization of the ATPase reaction cycle of endosomal AAA protein Vps4. J Mol Biol 2007; 374:655-70; PMID: 17949747; DOI: 10.1016/j.jmb.2007.09.067.
11. Nikko E, Andre B. Split-ubiquitin two-hybrid assay to analyze protein-protein interactions at the endosome: application to Saccharomyces cerevisiae Bro1 interacting with ESCRT complexes, the Doa4 ubiquitin hydrolase, and the Rsp5 ubiquitin ligase. Eukaryot Cell 2007; 6:1266-77; PMID: 17513562; DOI: 10.1128/EC.00024-07.
12. Vajjhala PR, Catchpoole E, Nguyen CH, Kistler C, Munn AL. Vps4 regulates a subset of protein interactions at the multivesicular endosome. FEBS J 2007; 274:1894-907; PMID: 17408385; DOI: 10.1111/j.1742-4658.2007.05736.x.
13. Xiao J, Xia H, Zhou J, Azmi IF, Davies BA, Katzmann DJ, et al. Structural basis of Vta1 function in the multivesicular body sorting pathway. Dev Cell 2008; 14:37-49; PMID: 18194651; DOI: 10.1016/j.devcel.2007.10.013.
14. Jäger S, Gottwein E, Krausslich HG. Ubiquitination of human immunodeficiency virus type 1 Gag is highly dependent on Gag membrane association. J Virol 2007; 81:9193-201; PMID: 17609272; DOI: 10.1128/JVI.00044-07.
15. Kyuuma M, Kikuchi K, Kojima K, Sugawara Y, Sato M, Mano N, et al. AMSH, an ESCRT-III associated enzyme, deubiquitinates cargo on MVB/late endosomes. Cell Struct Funct 2007; 31:159-72; PMID: 17159328; DOI: 10.1247/csf.06023.
16. Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, Hummer G, et al. The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev Cell 2007; 12:973-86; PMID: 17543868; DOI: 10.1016/j.devcel.2007. 04.013.
17. Row PE, Liu H, Hayes S, Welchman R, Charalabous P, Hofmann K, et al. The MIT domain of UBPY constitutes a CHMP binding and endosomal localization signal required for efficient epidermal growth factor receptor degradation. J Biol Chem 2007; 282:30929-37; PMID: 17711858; DOI: 10.1074/jbc.M704009200.
18. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, et al. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001; 107:55-65; PMID: 11595185; DOI: 10.1016/S0092-8674(01)00506- 2.
19. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, et al. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 2001; 98:7724-9; PMID: 11427703; DOI: 10.1073/pnas.131059198.
20. Carlton JG, Agromayor M, Martin-Serrano J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci USA 2008; 105:10541-6; PMID: 18641129; DOI: 10.1073/pnas.0802008105.
21. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, Rodesch CK, et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 2007; 26:4215-27; PMID: 17853893; DOI: 10.1038/sj.emboj.7601850.
22. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, Bechtold N, et al. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 2006; 133:4679-89; PMID: 17090720; DOI: 10.1242/dev.02654.
23. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH. Membrane scission by the ESCRT-III complex. Nature 2009; 458:172-7; PMID: 19234443; DOI: 10.1038/nature07836.
24. Stuffers S, Brech A, Stenmark H. ESCRT proteins in physiology and disease. Exp Cell Res 2009; 315:1619-26; PMID: 19013455; DOI: 10.1016/j.yexcr.2008.10.013.
25. Li L, Cohen SN. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 1996; 85:319-29; PMID: 8616888; DOI: 10.1016/S0092-8674(00)81111-3.
26. Lu Q, Hope LW, Brasch M, Reinhard C, Cohen SN. TSG101 interaction with HRS mediates endosomal trafficking and receptor downregulation. Proc Natl Acad Sci USA 2003; 100:7626-31; PMID: 12802020; DOI: 10.1073/pnas.0932599100.
27. Bache KG, Slagsvold T, Cabezas A, Rosendal KR, Raiborg C, Stenmark H. The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor downregulation. Mol Biol Cell 2004; 15:4337-46; PMID: 15240819; DOI: 10.1091/mbc.E04-03-0250.
28. Vaccari T, Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev Cell 2005; 9:687-98; PMID: 16256743; DOI: 10.1016/j.devcel.2005.09.019.
29. Bajorek M, Schubert HL, McCullough J, Langelier C, Eckert DM, Stubblefield WM, et al. Structural basis for ESCRT-III protein autoinhibition. Nat Struct Mol Biol 2009; 16:754-62; PMID: 19525971; DOI: 10.1038/nsmb.1621.
30. Shim S, Kimpler LA, Hanson PI. Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 2007; 8:1068-79; PMID: 17547705; DOI: 10.1111/j.1600-0854.2007.00584.x.
31. Shim S, Merrill SA, Hanson PI. Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly. Mol Biol Cell 2008; 19:2661-72; PMID: 18385515; DOI: 10.1091/mbc.E07-12-1263.
32. Shestakova A, Hanono A, Drosner S, Curtiss M, Davies BA, Katzmann DJ, et al. Assembly of the AAA ATPase Vps4 on ESCRT-III. Mol Biol Cell 2010; 21:1059-71; PMID: 20110351; DOI: 10.1091/mbc.E09-07-0572.
33. Davies BA, Azmi IF, Payne J, Shestakova A, Horazdovsky BF, Babst M, et al. Coordination of substrate binding and ATP hydrolysis in Vps4-mediated ESCRT-III disassembly. Mol Biol Cell 2010; 21:3396-408; PMID: 20702581; DOI: 10.1091/mbc.E10-06-0512.
34. Azmi IF, Davies BA, Xiao J, Babst M, Xu Z, Katzmann DJ. ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev Cell 2008; 14:50-61; PMID: 18194652; DOI: 10.1016/j.devcel.2007.10.021.
35. Howard TL, Stauffer DR, Degnin CR, Hollenberg SM. CHMP1 functions as a member of a newly defined family of vesicle trafficking proteins. J Cell Sci 2001; 114:2395-404; PMID: 11559748.
36. Bajorek M, Morita E, Skalicky JJ, Morham SG, Babst M, Sundquist WI. Biochemical analyses of human IST1 and its function in cytokinesis. Mol Biol Cell 2009; 20:1360-73; PMID: 19129479; DOI: 10.1091/mbc.E08-05-0475.
37. Rue SM, Mattei S, Saksena S, Emr SD. Novel Ist1- Did2 complex functions at a late step in multivesicular body sorting. Mol Biol Cell 2008; 19:475-84; PMID: 18032584; DOI: 10.1091/mbc.E07-07-0694.
38. Tsang HT, Connell JW, Brown SE, Thompson A, Reid E, Sanderson CM. A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics 2006; 88:333-46; PMID: 16730941; DOI: 10.1016/j.ygeno.2006.04. 003.
39. Stauffer DR, Howard TL, Nyun T, Hollenberg SM. CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell cycle progression. J Cell Sci 2001; 114:2383-93; PMID: 11559747.
40. Li J, Belogortseva N, Porter D, Park M. Chmp1A functions as a novel tumor suppressor gene in human embryonic kidney and ductal pancreatic tumor cells. Cell Cycle 2008; 7:2886-93; PMID: 18787405; DOI: 10.4161/cc.7.18.6677.
41. Li J, Orr B, White K, Belogortseva N, Niles R, Boskovic G, et al. Chmp 1A is a mediator of the antiproliferative effects of All-trans retinoic acid in human pancreatic cancer cells. Mol Cancer 2009; 8:7; PMID: 19216755; DOI: 10.1186/1476-4598-8-7.
42. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506; PMID: 12556884; DOI: 10.1038/nature01368.
43. Loehberg CR, Thompson T, Kastan MB, Maclean KH, Edwards DG, Kittrell FS, et al. Ataxia telangiectasia-mutated and p53 are potential mediators of chloroquine-induced resistance to mammary carcinogenesis. Cancer Res 2007; 67:12026-33; PMID: 18089834; DOI: 10.1158/0008-5472.CAN-07-3058.
44. Hitomi M, Yang K, Stacey AW, Stacey DW. Phosphorylation of cyclin D1 regulated by ATM or ATR controls cell cycle progression. Mol Cell Biol 2008; 28:5478-93; PMID: 18606783; DOI: 10.1128/MCB.02047-07.
45. Xu X, Tsvetkov LM, Stern DF. Chk2 activation and phosphorylation- dependent oligomerization. Mol Cell Biol 2002; 22:4419-32; PMID: 12024051; DOI: 10.1128/MCB.22.12.4419-32.2002.
46. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998; 281:1674-7; PMID: 9733514; DOI: 10.1126/science.281.5383.1674.
47. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998; 281:1677-9; PMID: 9733515; DOI: 10.1126/science.281.5383.1677.
48. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, Karnitz LM, et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999; 59:4375-82; PMID: 10485486.
49. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NM, Orr AI, et al. Identification and characterization of a novel and specific inhibitor of the ataxiatelangiectasia mutated kinase ATM. Cancer Res 2004; 64:9152-9; PMID: 15604286; DOI: 10.1158/0008-5472.CAN-04-2727.
50. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 2003; 81:123-9; PMID: 12897845; DOI: 10.1139/o03-042.
51. Butz J, Wickstrom E, Edwards J. Characterization of mutations and loss of heterozygosity of p53 and K-ras2 in pancreatic cancer cell lines by immobilized polymerase chain reaction. BMC Biotechnol 2003; 3:11; PMID: 12877750; DOI: 10.1186/1472-6750-3-11.