27
Views
11
CrossRef citations to date
0
Altmetric
Article

The Catalytic Activity of the Mitogen-Activated Protein Kinase Extracellular Signal-Regulated Kinase 3 Is Required To Sustain CD4+ CD8+ Thymocyte Survival

, , , , , , , , & show all
Pages 3374-3387 | Received 23 Dec 2013, Accepted 06 Jun 2014, Published online: 20 Mar 2023

REFERENCES

  • Pearson G, Robinson F, Gibson TB, Xu BE, Karandikar M, Berman K, Cobb MH. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:153–183. http://dx.doi.org/10.1210/edrv.22.2.0428.
  • Boulton TG, Nye SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD. 1991. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663–675. http://dx.doi.org/10.1016/0092-8674(91)90098-J.
  • Coulombe P, Meloche S. 2007. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim. Biophys. Acta 1773:1376–1387. http://dx.doi.org/10.1016/j.bbamcr.2006.11.001.
  • Deleris P, Rousseau J, Coulombe P, Rodier G, Tanguay PL, Meloche S. 2008. Activation loop phosphorylation of the atypical MAP kinases ERK3 and ERK4 is required for binding, activation and cytoplasmic relocalization of MK5. J. Cell. Physiol. 217:778–788. http://dx.doi.org/10.1002/jcp.21560.
  • Deleris P, Trost M, Topisirovic I, Tanguay PL, Borden KL, Thibault P, Meloche S. 2011. Activation loop phosphorylation of ERK3/ERK4 by group I p21-activated kinases (PAKs) defines a novel PAK-ERK3/4-MAPK-activated protein kinase 5 signaling pathway. J. Biol. Chem. 286:6470–6478. http://dx.doi.org/10.1074/jbc.M110.181529.
  • De la Mota-Peynado A, Chernoff J, Beeser A. 2011. Identification of the atypical MAPK Erk3 as a novel substrate for p21-activated kinase (Pak) activity. J. Biol. Chem. 286:13603–13611. http://dx.doi.org/10.1074/jbc.M110.181743.
  • Schumacher S, Laass K, Kant S, Shi Y, Visel A, Gruber AD, Kotlyarov A, Gaestel M. 2004. Scaffolding by ERK3 regulates MK5 in development. EMBO J. 23:4770–4779. http://dx.doi.org/10.1038/sj.emboj.7600467.
  • Seternes OM, Mikalsen T, Johansen B, Michaelsen E, Armstrong CG, Morrice NA, Turgeon B, Meloche S, Moens U, Keyse SM. 2004. Activation of MK5/PRAK by the atypical MAP kinase ERK3 defines a novel signal transduction pathway. EMBO J. 23:4780–4791. http://dx.doi.org/10.1038/sj.emboj.7600489.
  • Aberg E, Perander M, Johansen B, Julien C, Meloche S, Keyse SM, Seternes OM. 2006. Regulation of MAPK-activated protein kinase 5 activity and subcellular localization by the atypical MAPK ERK4/MAPK4. J. Biol. Chem. 281:35499–35510. http://dx.doi.org/10.1074/jbc.M606225200.
  • Kant S, Schumacher S, Singh MK, Kispert A, Kotlyarov A, Gaestel M. 2006. Characterization of the atypical MAPK ERK4 and its activation of the MAPK-activated protein kinase MK5. J. Biol. Chem. 281:35511–35519. http://dx.doi.org/10.1074/jbc.M606693200.
  • Gaestel M. 2006. MAPKAP kinases—MKs —two's company, three's a crowd. Nat. Rev. Mol. Cell Biol. 7:120–130. http://dx.doi.org/10.1038/nrm1834.
  • Perander M, Keyse SM, Seternes OM. 2008. Does MK5 reconcile classical and atypical MAP kinases? Front. Biosci. 13:4617–4624. http://dx.doi.org/10.2741/3027.
  • Chow KT, Timblin GA, McWhirter SM, Schlissel MS. 2013. MK5 activates Rag transcription via Foxo1 in developing B cells. J. Exp. Med. 210:1621–1634. http://dx.doi.org/10.1084/jem.20130498.
  • Coulombe P, Rodier G, Pelletier S, Pellerin J, Meloche S. 2003. Rapid turnover of extracellular signal-regulated kinase 3 by the ubiquitin-proteasome pathway defines a novel paradigm of mitogen-activated protein kinase regulation during cellular differentiation. Mol. Cell. Biol. 23:4542–4558. http://dx.doi.org/10.1128/MCB.23.13.4542-4558.2003.
  • Klinger S, Turgeon B, Levesque K, Wood GA, Aagaard-Tillery KM, Meloche S. 2009. Loss of Erk3 function in mice leads to intrauterine growth restriction, pulmonary immaturity, and neonatal lethality. Proc. Natl. Acad. Sci. U. S. A. 106:16710–16715. http://dx.doi.org/10.1073/pnas.0900919106.
  • Brand F, Schumacher S, Kant S, Menon MB, Simon R, Turgeon B, Britsch S, Meloche S, Gaestel M, Kotlyarov A. 2012. The extracellular signal-regulated kinase 3 (mitogen-activated protein kinase 6 [MAPK6])-MAPK-activated protein kinase 5 signaling complex regulates septin function and dendrite morphology. Mol. Cell. Biol. 32:2467–2478. http://dx.doi.org/10.1128/MCB.06633-11.
  • Bhandoola A, von Boehmer H, Petrie HT, Zuniga-Pflucker JC. 2007. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 26:678–689. http://dx.doi.org/10.1016/j.immuni.2007.05.009.
  • Hoffman ES, Passoni L, Crompton T, Leu TM, Schatz DG, Koff A, Owen MJ, Hayday AC. 1996. Productive T-cell receptor beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948–962. http://dx.doi.org/10.1101/gad.10.8.948.
  • Lin WC, Desiderio S. 1994. Cell cycle regulation of V(D)J recombination-activating protein RAG-2. Proc. Natl. Acad. Sci. U. S. A. 91:2733–2737. http://dx.doi.org/10.1073/pnas.91.7.2733.
  • Aifantis I, Mandal M, Sawai K, Ferrando A, Vilimas T. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol. Rev. 209:159–169. http://dx.doi.org/10.1111/j.0105-2896.2006.00343.x.
  • Starr TK, Jameson SC, Hogquist KA. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21:139–176. http://dx.doi.org/10.1146/annurev.immunol.21.120601.141107.
  • Labrecque N, Baldwin T, Lesage S. 2011. Molecular and genetic parameters defining T-cell clonal selection. Immunol. Cell Biol. 89:16–26. http://dx.doi.org/10.1038/icb.2010.119.
  • Bassing CH, Alt FW. 2004. The cellular response to general and programmed DNA double strand breaks. DNA Repair 3:781–796. http://dx.doi.org/10.1016/j.dnarep.2004.06.001.
  • Gellert M. 2002. V(D)J. recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 71:101–132. http://dx.doi.org/10.1146/annurev.biochem.71.090501.150203.
  • Rooney S, Chaudhuri J, Alt FW. 2004. The role of the non-homologous end-joining pathway in lymphocyte development. Immunol. Rev. 200:115–131. http://dx.doi.org/10.1111/j.0105-2896.2004.00165.x.
  • Guo J, Hawwari A, Li H, Sun Z, Mahanta SK, Littman DR, Krangel MS, He YW. 2002. Regulation of the TCRalpha repertoire by the survival window of CD4(+)CD8(+) thymocytes. Nat. Immunol. 3:469–476. http://dx.doi.org/10.1038/ni791.
  • Grillot DA, Merino R, Nunez G. 1995. Bcl-XL displays restricted distribution during T cell development and inhibits multiple forms of apoptosis but not clonal deletion in transgenic mice. J. Exp. Med. 182:1973–1983. http://dx.doi.org/10.1084/jem.182.6.1973.
  • Ma A, Pena JC, Chang B, Margosian E, Davidson L, Alt FW, Thompson CB. 1995. Bclx regulates the survival of double-positive thymocytes. Proc. Natl. Acad. Sci. U. S. A. 92:4763–4767. http://dx.doi.org/10.1073/pnas.92.11.4763.
  • D'Cruz LM, Knell J, Fujimoto JK, Goldrath AW. 2010. An essential role for the transcription factor HEB in thymocyte survival, Tcra rearrangement and the development of natural killer T cells. Nat. Immunol. 11:240–249. http://dx.doi.org/10.1038/ni.1845.
  • Hu T, Simmons A, Yuan J, Bender TP, Alberola-Ila J. 2010. The transcription factor c-Myb primes CD4+CD8+ immature thymocytes for selection into the iNKT lineage. Nat. Immunol. 11:435–441. http://dx.doi.org/10.1038/ni.1865.
  • Yuan J, Crittenden RB, Bender TP. 2010. c-Myb promotes the survival of CD4+CD8+ double-positive thymocytes through upregulation of Bcl-xL. J. Immunol. 184:2793–2804. http://dx.doi.org/10.4049/jimmunol.0902846.
  • Wang R, Xie H, Huang Z, Ma J, Fang X, Ding Y, Sun Z. 2011. T cell factor 1 regulates thymocyte survival via a RORgammat-dependent pathway. J. Immunol. 187:5964–5973. http://dx.doi.org/10.4049/jimmunol.1101205.
  • Fischer AM, Katayama CD, Pages G, Pouyssegur J, Hedrick SM. 2005. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 23:431–443. http://dx.doi.org/10.1016/j.immuni.2005.08.013.
  • Rousseau J, Klinger S, Rachalski A, Turgeon B, Deleris P, Vigneault E, Poirier-Heon JF, Davoli MA, Mechawar N, El Mestikawy S, Cermakian N, Meloche S. 2010. Targeted inactivation of Mapk4 in mice reveals specific nonredundant functions of Erk3/Erk4 subfamily mitogen-activated protein kinases. Mol. Cell. Biol. 30:5752–5763. http://dx.doi.org/10.1128/MCB.01147-10.
  • Lacombe MH, Hardy MP, Rooney J, Labrecque N. 2005. IL-7 receptor expression levels do not identify CD8+ memory T lymphocyte precursors following peptide immunization. J. Immunol. 175:4400–4407. http://dx.doi.org/10.4049/jimmunol.175.7.4400.
  • Chan S, Correia-Neves M, Dierich A, Benoist C, Mathis D. 1998. Visualization of CD4/CD8 T cell commitment. J. Exp. Med. 188:2321–2333. http://dx.doi.org/10.1084/jem.188.12.2321.
  • Schmitt TM, Zuniga-Pflucker JC. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749–756. http://dx.doi.org/10.1016/S1074-7613(02)00474-0.
  • Mathieu M, Cotta-Grand N, Daudelin JF, Boulet S, Lapointe R, Labrecque N. 2012. CD40-activated B cells can efficiently prime antigen-specific naive CD8 T cells to generate effector but not memory T cells. PLoS One 7:e30139. http://dx.doi.org/10.1371/journal.pone.0030139.
  • McMurry MT, Hernandez-Munain C, Lauzurica P, Krangel MS. 1997. Enhancer control of local accessibility to V(D)J. recombinase. Mol. Cell. Biol. 17:4553–4561.
  • Ismail IH, Hendzel MJ. 2008. The gamma-H2A.X: is it just a surrogate marker of double-strand breaks or much more? Environ. Mol. Mutagen. 49:73–82. http://dx.doi.org/10.1002/em.20358.
  • Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905–916. http://dx.doi.org/10.1083/jcb.146.5.905.
  • Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858–5868. http://dx.doi.org/10.1074/jbc.273.10.5858.
  • Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. 2000. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 275:9390–9395. http://dx.doi.org/10.1074/jbc.275.13.9390.
  • Yelamos J, Monreal Y, Saenz L, Aguado E, Schreiber V, Mota R, Fuente T, Minguela A, Parrilla P, de Murcia G, Almarza E, Aparicio P, Menissier-de Murcia J. 2006. PARP-2 deficiency affects the survival of CD4+CD8+ double-positive thymocytes. EMBO J. 25:4350–4360. http://dx.doi.org/10.1038/sj.emboj.7601301.
  • Dzhagalov I, Dunkle A, He YW. 2008. The anti-apoptotic Bcl-2 family member Mcl-1 promotes T lymphocyte survival at multiple stages. J. Immunol. 181:521–528. http://dx.doi.org/10.4049/jimmunol.181.1.521.
  • Boehm T, Scheu S, Pfeffer K, Bleul CC. 2003. Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbetaR. J. Exp. Med. 198:757–769. http://dx.doi.org/10.1084/jem.20030794.
  • Shores EW, Van Ewijk W, Singer A. 1991. Disorganization and restoration of thymic medullary epithelial cells in T cell receptor-negative scid mice: evidence that receptor-bearing lymphocytes influence maturation of the thymic microenvironment. Eur. J. Immunol. 21:1657–1661. http://dx.doi.org/10.1002/eji.1830210711.
  • van Ewijk W, Shores EW, Singer A. 1994. Crosstalk in the mouse thymus. Immunol. Today 15:214–217. http://dx.doi.org/10.1016/0167-5699(94)90246-1.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.