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Jan 10, 2022;14 (2):

Pathophysiological Integration of Metabolic Reprogramming in Breast Cancer.

Roberto Corchado-Cobos, Natalia García-Sancha, Marina Mendiburu-Eliçabe, Aurora Gómez-Vecino, Alejandro Jiménez-Navas, Manuel Jesús Pérez-Baena, Marina Holgado-Madruga, Jian-Hua Mao, Javier Cañueto, Sonia Castillo-Lluva, Jesús Pérez-Losada
Author Information
  1. Roberto Corchado-Cobos: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
  2. Natalia García-Sancha: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
  3. Marina Mendiburu-Eliçabe: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain.
  4. Aurora Gómez-Vecino: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain.
  5. Alejandro Jiménez-Navas: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
  6. Manuel Jesús Pérez-Baena: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
  7. Marina Holgado-Madruga: Instituto de Investigación Biosanitaria de Salamanca (IBSAL), 37007 Salamanca, Spain.
  8. Jian-Hua Mao: Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA. ORCID
  9. Javier Cañueto: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
  10. Sonia Castillo-Lluva: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Químicas, Universidad Complutense, 28040 Madrid, Spain. ORCID
  11. Jesús Pérez-Losada: Instituto de Biología Molecular y Celular del Cáncer (IBMCC-CIC), Universidad de Salamanca/CSIC, 37007 Salamanca, Spain. ORCID
PMID: 35053485 DOI: 10.3390/cancers14020322

Abstract

Metabolic changes that facilitate tumor growth are one of the hallmarks of cancer. The triggers of these metabolic changes are located in the tumor parenchymal cells, where oncogenic mutations induce an imperative need to proliferate and cause tumor initiation and progression. Cancer cells undergo significant metabolic reorganization during disease progression that is tailored to their energy demands and fluctuating environmental conditions. Oxidative stress plays an essential role as a trigger under such conditions. These metabolic changes are the consequence of the interaction between tumor cells and stromal myofibroblasts. The metabolic changes in tumor cells include protein anabolism and the synthesis of cell membranes and nucleic acids, which all facilitate cell proliferation. They are linked to catabolism and autophagy in stromal myofibroblasts, causing the release of nutrients for the cells of the tumor parenchyma. Metabolic changes lead to an interstitium deficient in nutrients, such as glucose and amino acids, and acidification by lactic acid. Together with hypoxia, they produce functional changes in other cells of the tumor stroma, such as many immune subpopulations and endothelial cells, which lead to tumor growth. Thus, immune cells favor tissue growth through changes in immunosuppression. This review considers some of the metabolic changes described in breast cancer.

Keywords

cancer-associated fibroblasts glucose hypoxia interstitium lactate macrophages metabolism

References

  1. Nat Commun. 2017 Jul 07;8:16031 [PMID: 28685754]
  2. Trends Endocrinol Metab. 2019 Jan;30(1):25-38 [PMID: 30471920]
  3. Blood. 2007 May 1;109(9):3812-9 [PMID: 17255361]
  4. J Gen Physiol. 1927 Mar 7;8(6):519-30 [PMID: 19872213]
  5. Nature. 2014 Oct 30;514(7524):628-32 [PMID: 25119024]
  6. Breast Cancer Res. 2010;12(6):R96 [PMID: 21080941]
  7. Oncogene. 2005 Sep 29;24(43):6465-81 [PMID: 16007182]
  8. Antioxid Redox Signal. 2012 Jun 1;16(11):1264-84 [PMID: 21883043]
  9. J Cancer. 2018 Jun 6;9(13):2308-2316 [PMID: 30026826]
  10. Curr Opin Immunol. 2006 Apr;18(2):220-5 [PMID: 16460921]
  11. Cancer Res. 1989 Dec 1;49(23):6449-65 [PMID: 2684393]
  12. Cell. 2015 Sep 10;162(6):1229-41 [PMID: 26321679]
  13. Cell Cycle. 2011 Aug 1;10(15):2504-20 [PMID: 21778829]
  14. Tumour Biol. 2016 Mar;37(3):4223-34 [PMID: 26493994]
  15. Proc Natl Acad Sci U S A. 2016 Sep 6;113(36):E5344-53 [PMID: 27543333]
  16. Trends Biochem Sci. 2014 Aug;39(8):347-54 [PMID: 25037503]
  17. Clin Cancer Res. 2007 May 1;13(9):2714-21 [PMID: 17473204]
  18. Cancer Res. 2012 Jan 15;72(2):560-7 [PMID: 22123926]
  19. Breast Cancer Res. 2009;11(4):R47 [PMID: 19589159]
  20. Semin Oncol. 2017 Jun;44(3):198-203 [PMID: 29248131]
  21. Cancer Res. 2000 Mar 15;60(6):1541-5 [PMID: 10749120]
  22. Cancer Sci. 2016 Dec;107(12):1730-1735 [PMID: 27727484]
  23. Cell. 2016 Oct 20;167(3):829-842.e13 [PMID: 27745970]
  24. Nat Rev Cancer. 2015 Jul;15(7):440-8 [PMID: 26084394]
  25. EMBO J. 2017 Aug 15;36(16):2334-2352 [PMID: 28659375]
  26. Nature. 2016 Aug 25;536(7617):479-83 [PMID: 27509858]
  27. Mol Cell. 2014 Jun 19;54(6):960-74 [PMID: 24857548]
  28. J Mol Med (Berl). 2011 Mar;89(3):229-36 [PMID: 21301794]
  29. Endocr Relat Cancer. 2013 May 21;20(3):339-48 [PMID: 23507704]
  30. Oncotarget. 2016 Nov 29;7(48):78396-78411 [PMID: 27623078]
  31. FASEB J. 2016 Nov;30(11):3800-3809 [PMID: 27492924]
  32. Mol Cell Proteomics. 2005 Nov;4(11):1686-96 [PMID: 16048908]
  33. Sci Rep. 2017 Nov 7;7(1):14749 [PMID: 29116138]
  34. J Clin Oncol. 2014 Sep 20;32(27):2959-66 [PMID: 25071121]
  35. Br J Cancer. 2017 Nov 21;117(11):1583-1591 [PMID: 29065107]
  36. Breast Cancer Res. 2019 Jan 17;21(1):7 [PMID: 30654824]
  37. Oncotarget. 2017 May 25;8(34):57813-57825 [PMID: 28915713]
  38. Oncogene. 2003 Jun 19;22(25):3937-42 [PMID: 12813467]
  39. Mol Biol Cell. 2013 Dec;24(23):3736-45 [PMID: 24088573]
  40. Nat Rev Drug Discov. 2011 Jun;10(6):417-27 [PMID: 21629292]
  41. Magn Reson Med. 2018 Sep;80(3):1138-1147 [PMID: 29327789]
  42. Cell Cycle. 2010 Sep 1;9(17):3506-14 [PMID: 20818174]
  43. Tumour Biol. 1987;8(5):251-63 [PMID: 3448771]
  44. Cell. 2013 Aug 1;154(3):651-63 [PMID: 23911327]
  45. Cell Metab. 2017 Feb 7;25(2):482 [PMID: 28178570]
  46. Expert Opin Ther Targets. 2017 Nov;21(11):1001-1016 [PMID: 28922023]
  47. Cell Metab. 2012 Jun 6;15(6):813-26 [PMID: 22682222]
  48. Trends Endocrinol Metab. 2008 Mar;19(2):65-73 [PMID: 18291668]
  49. Cell. 2011 Mar 4;144(5):646-74 [PMID: 21376230]
  50. J Cell Physiol. 2019 Feb;234(2):1768-1779 [PMID: 30132876]
  51. Mol Cell. 2016 Jan 21;61(2):210-21 [PMID: 26774282]
  52. J Exp Med. 1955 Jul 1;102(1):37-48 [PMID: 14392239]
  53. Cell Cycle. 2013 Sep 1;12(17):2723-32 [PMID: 23860382]
  54. Cancers (Basel). 2020 Jul 10;12(7): [PMID: 32664318]
  55. Clin Cancer Res. 2018 Jun 1;24(11):2482-2490 [PMID: 29420223]
  56. Cell. 2018 Aug 23;174(5):1054-1066 [PMID: 30142344]
  57. J Clin Oncol. 2006 Dec 1;24(34):5373-80 [PMID: 17135638]
  58. Neoplasia. 2003 Mar-Apr;5(2):135-45 [PMID: 12659686]
  59. Nature. 2017 Jan 19;541(7637):417-420 [PMID: 28077876]
  60. Cell. 2012 Jan 20;148(1-2):244-58 [PMID: 22265415]
  61. Mol Cell Endocrinol. 2018 Feb 15;462(Pt B):93-106 [PMID: 28119133]
  62. Histopathology. 2015 May;66(6):873-83 [PMID: 25387851]
  63. Nat Commun. 2017 Jan 10;8:13989 [PMID: 28071763]
  64. J Chromatogr B Analyt Technol Biomed Life Sci. 2015 Sep 1;1000:95-104 [PMID: 26218769]
  65. Nat Cell Biol. 2011 Feb;13(2):132-41 [PMID: 21258367]
  66. Oncotarget. 2016 Jun 28;7(26):40621-40629 [PMID: 27259254]
  67. Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14776-81 [PMID: 25267627]
  68. Dis Markers. 2018 Feb 25;2018:9369358 [PMID: 29682102]
  69. Science. 1955 Sep 16;122(3168):501-14 [PMID: 13255879]
  70. J Clin Oncol. 2013 Mar 1;31(7):860-7 [PMID: 23341518]
  71. Oncotarget. 2014 Nov 30;5(22):11029-37 [PMID: 25415228]
  72. Cancer Res. 2016 Jan 15;76(2):491-504 [PMID: 26744520]
  73. J Biol Chem. 2014 Mar 14;289(11):7884-96 [PMID: 24492615]
  74. Genes Dev. 2007 May 1;21(9):1037-49 [PMID: 17437992]
  75. Breast Cancer Res Treat. 2014 Jan;143(1):113-24 [PMID: 24309997]
  76. Nature. 2014 Sep 25;513(7519):559-63 [PMID: 25043024]
  77. Nature. 2011 Oct 05;478(7368):197-203 [PMID: 21976023]
  78. Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19345-50 [PMID: 18032601]
  79. Mol Endocrinol. 2011 Sep;25(9):1527-38 [PMID: 21835891]
  80. PLoS One. 2014 Jun 06;9(6):e98259 [PMID: 24906014]
  81. EMBO Rep. 2015 Oct;16(10):1394-408 [PMID: 26323721]
  82. PLoS One. 2017 Dec 6;12(12):e0188799 [PMID: 29211768]
  83. Oncotarget. 2017 May 16;8(20):33159-33171 [PMID: 28388539]
  84. Traffic. 2009 Apr;10(4):364-71 [PMID: 19192253]
  85. Clin Cancer Res. 2013 Feb 1;19(3):571-85 [PMID: 23236214]
  86. PLoS One. 2014 Nov 07;9(11):e112424 [PMID: 25380486]
  87. Eur J Surg Oncol. 2019 Jun;45(6):963-968 [PMID: 30745134]
  88. Cell Metab. 2013 Aug 6;18(2):153-61 [PMID: 23791484]
  89. J Immunol. 2010 Feb 1;184(3):1200-9 [PMID: 20026743]
  90. Pathol Oncol Res. 2012 Jul;18(3):721-8 [PMID: 22270867]
  91. Clin Immunol. 2010 Jun;135(3):466-75 [PMID: 20181533]
  92. Nat Rev Cancer. 2010 Jul;10(7):505-14 [PMID: 20574450]
  93. Science. 2002 May 31;296(5573):1655-7 [PMID: 12040186]
  94. Cell Biochem Biophys. 2012 Jan;62(1):153-9 [PMID: 22081436]
  95. Nat Chem Biol. 2017 May;13(5):494-500 [PMID: 28263965]
  96. Technol Cancer Res Treat. 2018 Jan 1;17:1533033818764499 [PMID: 29558872]
  97. PLoS One. 2013 Apr 16;8(4):e61991 [PMID: 23613998]
  98. Cell Metab. 2017 Jun 6;25(6):1282-1293.e7 [PMID: 28416194]
  99. Br J Cancer. 2009 May 5;100(9):1369-72 [PMID: 19352381]
  100. Kidney Int. 1997 Sep;52(3):637-47 [PMID: 9291182]
  101. Cancer Res. 2013 Oct 15;73(20):6164-74 [PMID: 24130112]
  102. Cancer Cell. 2007 Aug;12(2):108-13 [PMID: 17692803]
  103. Mol Cell Biol. 2005 Jul;25(14):6225-34 [PMID: 15988031]
  104. Exp Cell Res. 2017 Aug 15;357(2):211-221 [PMID: 28532652]
  105. Nat Commun. 2012;3:1271 [PMID: 23232401]
  106. PLoS One. 2014 Oct 23;9(10):e110928 [PMID: 25340823]
  107. Cancer Res. 2010 Jul 15;70(14):5728-39 [PMID: 20570887]
  108. Cancers (Basel). 2021 Nov 27;13(23): [PMID: 34885076]
  109. Cell Rep. 2016 May 10;15(6):1161-74 [PMID: 27134168]
  110. Nature. 2011 Jul 06;475(7354):106-9 [PMID: 21734707]
  111. Clin Cancer Res. 2005 Dec 1;11(23):8326-31 [PMID: 16322292]
  112. Cell Metab. 2016 Nov 8;24(5):657-671 [PMID: 27641098]
  113. Cell Cycle. 2010 Jun 15;9(12):2412-22 [PMID: 20562527]
  114. Cancer Metab. 2017 Aug 22;5:6 [PMID: 28852500]
  115. Cell Cycle. 2012 Aug 15;11(16):3019-35 [PMID: 22874531]
  116. Cancer Cell. 2015 Jan 12;27(1):57-71 [PMID: 25584894]
  117. Science. 2020 Apr 10;368(6487): [PMID: 32273439]
  118. Oncol Rep. 2014 Mar;31(3):1175-82 [PMID: 24366110]
  119. Nat Commun. 2021 Nov 10;12(1):6479 [PMID: 34759281]
  120. Oncogene. 2016 Jul 7;35(27):3535-43 [PMID: 26522726]
  121. Nat Rev Immunol. 2015 Jun;15(6):388-400 [PMID: 25998963]
  122. J Immunol. 2008 Apr 1;180(7):4476-86 [PMID: 18354169]
  123. Protein Cell. 2018 Feb;9(2):216-237 [PMID: 28748451]
  124. Nature. 2011 May 19;473(7347):298-307 [PMID: 21593862]
  125. J Clin Invest. 2013 Mar;123(3):1068-81 [PMID: 23426180]
  126. PLoS One. 2016 Apr 13;11(4):e0152500 [PMID: 27073890]
  127. J Biol Chem. 2006 Apr 7;281(14):9030-7 [PMID: 16452478]
  128. Cancer Res. 2011 May 1;71(9):3236-45 [PMID: 21415164]
  129. PLoS One. 2017 Apr 19;12(4):e0175755 [PMID: 28423034]
  130. Oncotarget. 2013 Dec;4(12):2502-11 [PMID: 24318446]
  131. Nat Genet. 2011 Jul 31;43(9):869-74 [PMID: 21804546]
  132. Cancer Lett. 2000 Dec 20;161(2):207-14 [PMID: 11090971]
  133. Int Immunol. 2006 Nov;18(11):1591-602 [PMID: 16987935]
  134. Nat Cell Biol. 2008 May;10(5):611-8 [PMID: 18391940]
  135. Br J Cancer. 2018 Jan;118(2):258-265 [PMID: 29169183]
  136. Proc Natl Acad Sci U S A. 2017 Jan 17;114(3):580-585 [PMID: 28049847]
  137. Oncotarget. 2017 Oct 7;8(63):106693-106706 [PMID: 29290982]
  138. Cancer Res. 1996 Oct 15;56(20):4625-9 [PMID: 8840975]
  139. Front Immunol. 2014 Oct 27;5:532 [PMID: 25386178]
  140. J Clin Invest. 2008 Dec;118(12):3930-42 [PMID: 19033663]
  141. Virchows Arch. 2017 Apr;470(4):381-389 [PMID: 28185053]
  142. Cancer Cell. 2013 Aug 12;24(2):213-228 [PMID: 23911236]
  143. Cancer Res. 2004 Jun 15;64(12):4270-6 [PMID: 15205341]
  144. Cancer Res. 2008 Feb 15;68(4):1003-11 [PMID: 18281474]
  145. Mol Biol Cell. 2002 Jul;13(7):2276-88 [PMID: 12134068]
  146. Oncotarget. 2014 Jun 30;5(12):4305-19 [PMID: 24946808]
  147. Cell. 2016 Jan 28;164(3):433-46 [PMID: 26824656]
  148. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):3948-53 [PMID: 10759542]
  149. Mol Oncol. 2018 Sep;12(9):1623-1638 [PMID: 30099850]
  150. Springerplus. 2013 Jul 03;2(1):299 [PMID: 23888270]
  151. Oncotarget. 2016 Sep 20;7(38):61890-61904 [PMID: 27542265]
  152. Mol Cell. 2010 Jul 30;39(2):171-83 [PMID: 20670887]
  153. Cancer Res. 2015 Oct 15;75(20):4312-21 [PMID: 26249173]
  154. Cell Cycle. 2013 Aug 15;12(16):2580-97 [PMID: 23860378]
  155. Hum Pathol. 2008 Jun;39(6):857-65 [PMID: 18400253]
  156. Cancer Res. 2011 Apr 1;71(7):2550-60 [PMID: 21300765]
  157. Cell Metab. 2018 Nov 6;28(5):793-800.e2 [PMID: 30146487]
  158. Cancer Cell. 2010 Dec 14;18(6):553-67 [PMID: 21130701]
  159. Cell. 2015 Sep 10;162(6):1217-28 [PMID: 26321681]
  160. Int J Obes (Lond). 2008 Sep;32 Suppl 4:S36-41 [PMID: 18719597]
  161. PLoS One. 2017 Sep 26;12(9):e0185092 [PMID: 28950000]
  162. Biosci Rep. 2018 Aug 29;38(4): [PMID: 30026261]
  163. Breast Cancer Res Treat. 2016 Nov;160(1):29-40 [PMID: 27613609]
  164. Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6436-41 [PMID: 20308543]
  165. BMC Genomics. 2012 Jul 23;13:334 [PMID: 22823888]
  166. Biochem J. 2000 Aug 15;350 Pt 1:219-27 [PMID: 10926847]
  167. Oncogenesis. 2020 May 15;9(5):51 [PMID: 32415061]
  168. Cell Metab. 2018 Oct 2;28(4):573-587.e13 [PMID: 30017355]
  169. Oncotarget. 2017 Nov 30;8(66):110426-110443 [PMID: 29299159]
  170. Cancer Res. 2012 Oct 1;72(19):5130-40 [PMID: 22850421]
  171. Nat Rev Cancer. 2014 Nov;14(11):754-62 [PMID: 25291291]
  172. Nat Rev Cancer. 2013 Aug;13(8):572-83 [PMID: 23822983]
  173. Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18782-7 [PMID: 19033189]
  174. Cell. 2009 Feb 6;136(3):521-34 [PMID: 19203585]
  175. Cell Cycle. 2012 Dec 1;11(23):4402-13 [PMID: 23172369]
  176. Oncogene. 2009 Oct 22;28(42):3689-701 [PMID: 19668225]
  177. Cell Cycle. 2009 Dec;8(23):3984-4001 [PMID: 19923890]
  178. Cancer Res. 2004 Apr 1;64(7):2627-33 [PMID: 15059920]
  179. Nat Cell Biol. 2011 Mar;13(3):310-6 [PMID: 21336310]
  180. Cell Cycle. 2010 May 15;9(10):1960-71 [PMID: 20495363]
  181. J Intern Med. 2016 Jun;279(6):541-62 [PMID: 26748421]
  182. Oncogene. 2018 Nov;37(45):5997-6009 [PMID: 29985480]
  183. Cell Metab. 2015 Oct 6;22(4):590-605 [PMID: 26365176]
  184. Clin Cancer Res. 2004 Nov 15;10(22):7466-74 [PMID: 15569976]
  185. Pathobiology. 2013;80(1):41-52 [PMID: 22832328]
  186. J Immunol. 2006 Oct 15;177(8):4962-5 [PMID: 17015677]
  187. FASEB J. 2018 Jan;32(1):276-288 [PMID: 28899878]
  188. Carcinogenesis. 2014 Nov;35(11):2567-75 [PMID: 25123132]
  189. Cancer Cell. 2014 Jul 14;26(1):121-135 [PMID: 25002027]
  190. Curr Opin Immunol. 2017 Apr;45:43-51 [PMID: 28192720]
  191. Cancer Res. 2011 Apr 1;71(7):2455-65 [PMID: 21459803]
  192. Cancer Res. 1994 Jul 1;54(13):3333-6 [PMID: 8012945]
  193. Nat Rev Cancer. 2007 Oct;7(10):763-77 [PMID: 17882277]
  194. Prog Lipid Res. 2018 Jan;69:11-20 [PMID: 29175445]
  195. Nature. 1996 Jan 4;379(6560):88-91 [PMID: 8538748]
  196. J Cell Biochem. 2008 Dec 1;105(5):1147-52 [PMID: 18814184]
  197. Breast Cancer Res. 2014 Aug 05;16(4):415 [PMID: 25091696]
  198. Cancer Res. 2012 Jun 1;72(11):2746-56 [PMID: 22593198]
  199. Nat Immunol. 2013 Nov;14(11):1173-82 [PMID: 24076634]
  200. Mol Cell Biol. 2003 Dec;23(24):9361-74 [PMID: 14645546]
  201. Mol Cell Biol. 2003 Oct;23(20):7315-28 [PMID: 14517300]
  202. PLoS One. 2012;7(12):e50946 [PMID: 23284651]
  203. J Immunol. 2011 Mar 15;186(6):3299-303 [PMID: 21317389]
  204. Mol Cell Biol. 2005 Nov;25(21):9543-53 [PMID: 16227604]
  205. Cell Rep. 2015 Mar 3;10(8):1335-48 [PMID: 25732824]
  206. Cell Metab. 2017 Dec 5;26(6):817-829.e6 [PMID: 28988820]
  207. Genes Dev. 2012 Sep 1;26(17):1926-44 [PMID: 22899010]
  208. Nat Rev Cancer. 2016 Oct;16(10):650-62 [PMID: 27634448]
  209. Cancer Cell. 2009 Sep 8;16(3):183-94 [PMID: 19732719]
  210. Cell Cycle. 2012 Mar 15;11(6):1108-17 [PMID: 22313602]
  211. J Steroid Biochem Mol Biol. 2015 May;149:118-27 [PMID: 25683269]
  212. Kidney Int. 2000 Dec;58(6):2351-66 [PMID: 11115069]
  213. Nature. 2019 Nov;575(7782):380-384 [PMID: 31666695]
  214. Br J Cancer. 2021 Jan;124(1):115-123 [PMID: 33204029]
  215. Science. 2017 Nov 17;358(6365):941-946 [PMID: 29025995]
  216. Mol Metab. 2020 Mar;33:102-121 [PMID: 31399389]
  217. Science. 2019 Nov 22;366(6468):1013-1021 [PMID: 31699883]
  218. Clin Cancer Res. 2015 Nov 15;21(22):5047-56 [PMID: 26567364]
  219. J Exp Med. 1996 Apr 1;183(4):1323-9 [PMID: 8666890]
  220. Cell. 2015 Apr 23;161(3):595-609 [PMID: 25892225]
  221. Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):5425-30 [PMID: 25870263]
  222. Sci Transl Med. 2015 Feb 11;7(274):274ra17 [PMID: 25673762]
  223. BMC Cancer. 2020 Apr 23;20(1):347 [PMID: 32326897]
  224. Nat Rev Cancer. 2015 Apr;15(4):225-37 [PMID: 25801618]
  225. Cell. 2003 Mar 7;112(5):645-57 [PMID: 12628185]
  226. Nature. 2013 May 30;497(7451):633-7 [PMID: 23665962]
  227. Cancer Res. 2010 Feb 1;70(3):859-62 [PMID: 20086171]
  228. Oncol Lett. 2016 Mar;11(3):1980-1986 [PMID: 26998110]
  229. Nature. 2017 Jan 5;541(7635):41-45 [PMID: 27974793]
  230. Dev Cell. 2016 Mar 7;36(5):540-9 [PMID: 26954548]
  231. Nat Med. 2018 Aug;24(8):1192-1203 [PMID: 29988124]
  232. Cell Cycle. 2010 Sep 1;9(17):3515-33 [PMID: 20855962]
  233. J Clin Invest. 2014 Jan;124(1):398-412 [PMID: 24316975]
  234. Exp Cell Res. 2012 Feb 15;318(4):326-35 [PMID: 22178238]
  235. Cancer Biol Ther. 2011 Nov 15;12(10):924-38 [PMID: 22041887]
  236. Cell Rep. 2016 Aug 9;16(6):1614-1628 [PMID: 27477280]
  237. Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16259-64 [PMID: 21930938]
  238. Int J Cancer. 2012 Aug 1;131(3):633-40 [PMID: 21898391]
  239. Front Oncol. 2020 Aug 19;10:1333 [PMID: 32974131]
  240. Cancer Res. 2000 Feb 15;60(4):916-21 [PMID: 10706105]
  241. J Oncol Pract. 2010 Jul;6(4):195-7 [PMID: 21037871]
  242. Circ Res. 2002 Oct 4;91(7):e4-12 [PMID: 12364394]
  243. Nat Med. 2001 Oct;7(10):1111-7 [PMID: 11590433]
  244. Cancer Epidemiol Biomarkers Prev. 2003 Dec;12(12):1486-91 [PMID: 14693742]
  245. J Transl Med. 2014 Dec 14;12:354 [PMID: 25496516]
  246. Int J Oncol. 2011 Aug;39(2):453-63 [PMID: 21617859]
  247. Cell Rep. 2020 Feb 25;30(8):2743-2757.e5 [PMID: 32101749]
  248. Cell Metab. 2008 Sep;8(3):224-36 [PMID: 18762023]
  249. Mol Cell Biol. 2002 Oct;22(20):7004-14 [PMID: 12242281]
  250. Trends Cell Biol. 2010 Jul;20(7):427-34 [PMID: 20399660]
  251. Cell Cycle. 2012 Nov 1;11(21):3956-63 [PMID: 23082721]
  252. EMBO J. 2017 Aug 15;36(16):2321-2333 [PMID: 28659379]
  253. Sci Rep. 2018 Jun 21;8(1):9482 [PMID: 29930291]
  254. BMC Cancer. 2012 Jul 23;12:306 [PMID: 22824040]
  255. Int J Cancer. 2003 Nov 1;107(2):177-82 [PMID: 12949791]
  256. J Natl Cancer Inst. 2003 Oct 1;95(19):1482-5 [PMID: 14519755]
  257. Sci Signal. 2015 Sep 29;8(396):ra97 [PMID: 26420908]
  258. Cell Metab. 2016 Nov 8;24(5):701-715 [PMID: 27773694]
  259. Mol Cancer. 2018 Jul 16;17(1):100 [PMID: 30012170]
  260. Theranostics. 2018 Oct 29;8(19):5452-5468 [PMID: 30555557]
  261. Science. 2017 Mar 24;355(6331):1324-1330 [PMID: 28336670]
  262. Proc Natl Acad Sci U S A. 2017 Mar 14;114(11):2934-2939 [PMID: 28246332]
  263. J Exp Clin Cancer Res. 2019 May 28;38(1):223 [PMID: 31138258]
  264. Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16062-7 [PMID: 21900605]
  265. PLoS Genet. 2011 Aug;7(8):e1002229 [PMID: 21852960]
  266. J Transl Med. 2015 Jun 04;13:180 [PMID: 26040463]
  267. Nature. 2011 Aug 18;476(7360):346-50 [PMID: 21760589]
  268. Eur J Cancer. 2019 Nov;121:154-171 [PMID: 31581056]
  269. Cancer Cell. 2016 Dec 12;30(6):968-985 [PMID: 27866851]
  270. Blood. 2004 Oct 15;104(8):2224-34 [PMID: 15231578]
  271. Nat Rev Cancer. 2021 Dec;21(12):753-766 [PMID: 34417571]
  272. Nat Med. 2018 Jul;24(7):1036-1046 [PMID: 29892070]
  273. Nat Rev Drug Discov. 2014 Feb;13(2):140-56 [PMID: 24481312]
  274. Cancer Immunol Immunother. 2005 Sep;54(9):898-906 [PMID: 15776284]
  275. J Immunol. 2015 Mar 15;194(6):2683-95 [PMID: 25694611]
  276. J Cell Biochem. 2012 Apr;113(4):1142-51 [PMID: 22095586]
  277. PLoS One. 2015 Mar 09;10(3):e0119473 [PMID: 25751270]
  278. J Biol Chem. 1994 Sep 23;269(38):23757-63 [PMID: 8089148]
  279. Nature. 2015 Jan 15;517(7534):293-301 [PMID: 25592534]
  280. Cell Cycle. 2011 Jun 1;10(11):1772-83 [PMID: 21558814]
  281. Cell Rep. 2017 Dec 26;21(13):3819-3832 [PMID: 29281830]
  282. PLoS One. 2008 Jul 16;3(7):e2722 [PMID: 18628958]
  283. Oncol Lett. 2013 Dec;6(6):1701-1706 [PMID: 24260065]
  284. J Immunol. 2010 Jul 15;185(2):1037-44 [PMID: 20554958]
  285. Nat Commun. 2017 Mar 10;8:14706 [PMID: 28281525]
  286. Exp Cell Res. 2017 Mar 1;352(1):20-33 [PMID: 28132882]
  287. Cell. 2006 Jul 14;126(1):107-20 [PMID: 16839880]
  288. Nature. 2009 Apr 9;458(7239):762-5 [PMID: 19219026]
  289. Mol Endocrinol. 2012 Dec;26(12):2058-70 [PMID: 23028062]
  290. J Invest Dermatol. 2010 Dec;130(12):2818-27 [PMID: 20686497]
  291. N Engl J Med. 2010 Mar 11;362(10):875-85 [PMID: 20220182]
  292. Nat Med. 1997 Feb;3(2):177-82 [PMID: 9018236]
  293. PLoS One. 2013 Sep 12;8(9):e75154 [PMID: 24069390]
  294. Oncotarget. 2017 Mar 7;8(10):16875-16886 [PMID: 28187435]
  295. Cell. 2017 Oct 5;171(2):358-371.e9 [PMID: 28985563]
  296. Amino Acids. 2012 Jan;42(1):231-46 [PMID: 21409388]
  297. PLoS One. 2014 May 27;9(5):e97697 [PMID: 24866893]
  298. Proc Natl Acad Sci U S A. 2013 May 28;110(22):8882-7 [PMID: 23671091]
  299. Cancer Res. 2015 Feb 1;75(3):544-53 [PMID: 25644265]
  300. Cancer Cell. 2017 Sep 11;32(3):377-391.e9 [PMID: 28898698]
  301. MAGMA. 1998 Aug;6(1):44-52 [PMID: 9794289]
  302. Breast Cancer Res. 2015 Aug 05;17:101 [PMID: 26243145]
  303. Biomed Res Int. 2015;2015:960840 [PMID: 26171396]
  304. Science. 1956 Feb 24;123(3191):309-14 [PMID: 13298683]
  305. Oncogene. 1998 Aug 13;17(6):769-80 [PMID: 9715279]
  306. Cell. 2016 Feb 11;164(4):681-94 [PMID: 26853473]

Grants

  1. PID2020-118527RB-I00/Ministerio de Ciencia e Innovación
  2. PDC2021-121735-I00/Ministerio de Ciencia e Innovación
  3. PIE14/00066/Carlos III Health Institute
  4. CSI234P18/Regional Government of Castile and León
  5. CSI144P20/Regional Government of Castile and León
  6. RTI2018-094130-B-100/Ministerio de Ciencia e Innovación
  7. SAF2014-56989-R/Ministerio de Economía, Industria y Competitividad
  8. SAF2017-88854R/Ministerio de Economía, Industria y Competitividad
  9. GRS2139/A/20/Gerencia Regional de Salud de Castilla y León
  10. PI18/00587/Instituto de Salud Carlos III
  11. PI21/01207/Instituto de Salud Carlos III
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