Regulation of Hematopoiesis and Methionine Homeostasis by mTORC1 Inhibitor NPRL2

Cell Reports

Volumn 12, Issue 3, 2015, Pages 371-379

  Dutchak, Paul A ^a   Laxman, Sunil ^a   Estill, Sandi Jo ^a   Wang, Chensu ^b   Wang, Yun ^a   Wang, Yiguang ^b   Bulut, Gamze B ^c   Gao, Jinming ^b   Huang, Lily J ^c   Tu, Benjamin P ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COBALAMIN; HOMOCYSTEINE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; METHIONINE; METHIONINE SYNTHASE; NITROGEN PERMEASE REGULATOR LIKE 2 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE; TUMOR SUPPRESSOR PROTEIN;

ACIDIFICATION; AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FETUS; HEMATOPOIESIS; LYSOSOME; METABOLIC REGULATION; METABOLITE; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; FEMALE; HEMATOPOIESIS; METHIONINE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84937512734     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.042     Document Type: Article

References (50)

1. Agrawal V., Alpini S.E., Stone E.M., Frenkel E.P., Frankel A.E. Targeting methionine auxotrophy in cancer: discovery & exploration. Expert Opin. Biol. Ther. 2012, 12:53-61.
2. Akaike A., Tamura Y., Sato Y., Yokota T. Protective effects of a vitamin B12 analog, methylcobalamin, against glutamate cytotoxicity in cultured cortical neurons. Eur. J. Pharmacol. 1993, 241:1-6.
3. Banerjee R.V., Matthews R.G. Cobalamin-dependent methionine synthase. FASEB J. 1990, 4:1450-1459.
4. Bar-Peled L., Chantranupong L., Cherniack A.D., Chen W.W., Ottina K.A., Grabiner B.C., Spear E.D., Carter S.L., Meyerson M., Sabatini D.M. A tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 2013, 340:1100-1106.
5. Carmel R., Green R., Rosenblatt D.S., Watkins D. Update on cobalamin, folate, and homocysteine. Hematology 2003, 62-81.
6. Chen C., Liu Y., Liu R., Ikenoue T., Guan K.L., Liu Y., Zheng P. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J.Exp. Med. 2008, 205:2397-2408.
7. Dibbens L.M., de Vries B., Donatello S., Heron S.E., Hodgson B.L., Chintawar S., Crompton D.E., Hughes J.N., Bellows S.T., Klein K.M., et al. Mutations in DEPDC5 cause familial focal epilepsy with variable foci. Nat. Genet. 2013, 45:546-551.
8. Dibble C.C., Manning B.D. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat. Cell Biol. 2013, 15:555-564.
9. Dokudovskaya S., Waharte F., Schlessinger A., Pieper U., Devos D.P., Cristea I.M., Williams R., Salamero J., Chait B.T., Sali A., et al. A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae. Mol. Cell. Proteomics 2011, 10. M110 006478.
10. Efeyan A., Zoncu R., Chang S., Gumper I., Snitkin H., Wolfson R.L., Kirak O., Sabatini D.D., Sabatini D.M. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 2013, 493:679-683.
11. Gan B., Sahin E., Jiang S., Sanchez-Aguilera A., Scott K.L., Chin L., Williams D.A., Kwiatkowski D.J., DePinho R.A. mTORC1-dependent and -independent regulation of stem cell renewal, differentiation, and mobilization. Proc. Natl. Acad. Sci. USA 2008, 105:19384-19389.
12. Glaudemans A.W., Enting R.H., Heesters M.A., Dierckx R.A., van Rheenen R.W., Walenkamp A.M., Slart R.H. Value of 11C-methionine PET in imaging brain tumours and metastases. Eur. J. Nucl. Med. Mol. Imaging 2013, 40:615-635.
13. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
14. Herbert V., Zalusky R. Interrelations of vitamin B12 and folic acidmetabolism: folic acid clearance studies. J.Clin. Invest. 1962, 41:1263-1276.
15. Inoki K., Li Y., Zhu T., Wu J., Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 2002, 4:648-657.
16. Inoki K., Corradetti M.N., Guan K.L. Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 2005, 37:19-24.
17. Kim Y.C., Park H.W., Sciarretta S., Mo J.S., Jewell J.L., Russell R.C., Wu X., Sadoshima J., Guan K.L. Rag GTPases are cardioprotective by regulating lysosomal function. Nat. Commun. 2014, 5:4241.
18. Kira S., Tabata K., Shirahama-Noda K., Nozoe A., Yoshimori T., Noda T. Reciprocal conversion of Gtr1 and Gtr2 nucleotide-binding states byNpr2-Npr3 inactivates TORC1 and induces autophagy. Autophagy 2014, 10:1565-1578.
19. Klee G.G. Cobalamin and folate evaluation: measurement of methylmalonic acid and homocysteine vs vitamin B(12) and folate. Clin. Chem. 2000, 46:1277-1283.
20. Knight Z.A., Schmidt S.F., Birsoy K., Tan K., Friedman J.M. A critical role for mTORC1 in erythropoiesis and anemia. eLife 2014, 3:e01913.
21. Koury M.J., Ponka P. New insights into erythropoiesis: the roles offolate, vitamin B12, and iron. Annu. Rev. Nutr. 2004, 24:105-131.
22. Kowalczyk M.S., Hughes J.R., Garrick D., Lynch M.D., Sharpe J.A., Sloane-Stanley J.A., McGowan S.J., De Gobbi M., Hosseini M., Vernimmen D., et al. Intragenic enhancers act as alternative promoters. Mol. Cell 2012, 45:447-458.
23. Kumar S. Recurrent seizures: an unusual manifestation of vitamin B12 deficiency. Neurol. India 2004, 52:122-123.
24. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
25. Laxman S., Sutter B.M., Wu X., Kumar S., Guo X., Trudgian D.C., Mirzaei H., Tu B.P. Sulfur amino acids regulate translational capacity andmetabolic homeostasis through modulation of tRNA thiolation. Cell 2013, 154:416-429.
26. Laxman S., Sutter B.M., Shi L., Tu B.P. Npr2 inhibits TORC1 toprevent inappropriate utilization of glutamine for biosynthesis of nitrogen-containing metabolites. Sci. Signal. 2014, 7:ra120.
27. Lerman M.I., Minna J.D. The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Res. 2000, 60:6116-6133.
28. Li J., Wang F., Haraldson K., Protopopov A., Duh F.M., Geil L., Kuzmin I., Minna J.D., Stanbridge E., Braga E., et al. Functional characterization of the candidate tumor suppressor gene NPRL2/G21 located in 3p21.3C. Cancer Res. 2004, 64:6438-6443.
29. Ma X., Wang Y., Zhao T., Li Y., Su L.C., Wang Z., Huang G., Sumer B.D., Gao J. Ultra-pH-sensitive nanoprobe library with broad pH tunability and fluorescence emissions. J.Am. Chem. Soc. 2014, 136:11085-11092.
30. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 2002, 10:151-162.
31. Mindell J.A. Lysosomal acidification mechanisms. Annu. Rev. Physiol. 2012, 74:69-86.
32. Neklesa T.K., Davis R.W. A genome-wide screen for regulators ofTORC1 in response to amino acid starvation reveals a conserved Npr2/3 complex. PLoS Genet. 2009, 5:e1000515.
33. Panchaud N., Péli-Gulli M.P., De Virgilio C. Amino acid deprivation inhibits TORC1 through a GTPase-activating protein complex for the Rag family GTPase Gtr1. Sci. Signal. 2013, 6:ra42.
34. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., Ferguson S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 2012, 5:ra42.
35. Rosenblatt D.S., Hosack A., Matiaszuk N.V., Cooper B.A., Laframboise R. Defect in vitamin B12 release from lysosomes: newly described inborn error of vitamin B12 metabolism. Science 1985, 228:1319-1321.
36. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Di Malta C., Donaudy F., Embrione V., Polishchuk R.S., et al. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.
37. Scott J.M., Weir D.G. The methyl folate trap. A physiological response in man to prevent methyl group deficiency in kwashiorkor (methionine deficiency) and an explanation for folic-acid induced exacerbation of subacute combined degeneration in pernicious anaemia. Lancet 1981, 2:337-340.
38. Shimobayashi M., Hall M.N. Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat. Rev. Mol. Cell Biol. 2014, 15:155-162.
39. Shiraki N., Shiraki Y., Tsuyama T., Obata F., Miura M., Nagae G., Aburatani H., Kume K., Endo F., Kume S. Methionine metabolism regulates maintenance and differentiation of human pluripotent stem cells. Cell Metab. 2014, 19:780-794.
40. Stabler S.P. Vitamin B12 deficiency. N.Engl. J. Med. 2013, 368:2041-2042.
41. Steingrímsson E., Moore K.J., Lamoreux M.L., Ferré-D'Amaré A.R., Burley S.K., Zimring D.C., Skow L.C., Hodgkinson C.A., Arnheiter H., Copeland N.G., et al. Molecular basis of mouse microphthalmia (mi) mutations helps explain their developmental and phenotypic consequences. Nat. Genet. 1994, 8:256-263.
42. Sutter B.M., Wu X., Laxman S., Tu B.P. Methionine inhibits autophagy and promotes growth by inducing the SAM-responsive methylation of PP2A. Cell 2013, 154:403-415.
43. Tee A.R., Fingar D.C., Manning B.D., Kwiatkowski D.J., Cantley L.C., Blenis J. Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc. Natl. Acad. Sci. USA 2002, 99:13571-13576.
44. Watkins D., Rosenblatt D.S. Lessons in biology from patients withinborn errors of vitamin B12 metabolism. Biochimie 2013, 95:1019-1022.
45. Wu X., Tu B.P. Selective regulation of autophagy by the Iml1-Npr2-Npr3 complex in the absence of nitrogen starvation. Mol. Biol. Cell 2011, 22:4124-4133.
46. Yilmaz O.H., Valdez R., Theisen B.K., Guo W., Ferguson D.O., Wu H., Morrison S.J. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006, 441:475-482.
47. Youngdahl-Turner P., Rosenberg L.E., Allen R.H. Binding and uptake of transcobalamin II by human fibroblasts. J.Clin. Invest. 1978, 61:133-141.
48. Zhang J., Socolovsky M., Gross A.W., Lodish H.F. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood 2003, 102:3938-3946.
49. Zhou K., Wang Y., Huang X., Luby-Phelps K., Sumer B.D., Gao J. Tunable, ultrasensitive pH-responsive nanoparticles targeting specific endocytic organelles in living cells. Angew. Chem. Int. Ed. Engl. 2011, 50:6109-6114.
50. Zhou J., Tan S.H., Nicolas V., Bauvy C., Yang N.D., Zhang J., Xue Y., Codogno P., Shen H.M. Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res. 2013, 23:508-523.