Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Mitogen-activated protein kinases in apoptosis regulation

Oncogene volume 23, pages 2838–2849 (2004)Cite this article

Abstract

Cells are continuously exposed to a variety of environmental stresses and have to decide ‘to be or not to be’ depending on the types and strength of stress. Among the many signaling pathways that respond to stress, mitogen-activated protein kinase (MAPK) family members are crucial for the maintenance of cells. Three subfamilies of MAPKs have been identified: extracellular signal-regulated kinases (ERKs), c-Jun N-terminal kinases (JNKs), and p38-MAPKs. It has been originally shown that ERKs are important for cell survival, whereas JNKs and p38-MAPKs were deemed stress responsive and thus involved in apoptosis. However, the regulation of apoptosis by MAPKs is more complex than initially thought and often controversial. In this review, we discuss MAPKs in apoptosis regulation with attention to mouse genetic models and critically point out the multiple roles of MAPKs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  • Abe MK, Kahle KT, Saelzler MP, Orth K, Dixon JE and Rosner MR . (2001). J. Biol. Chem., 276, 21272–21279.

  • Abe MK, Kuo WL, Hershenson MB and Rosner MR . (1999). Mol. Cell. Biol., 19, 1301–1312.

  • Abe MK, Saelzler MP, Espinosa III R, Kahle KT, Hershenson MB, Le Beau MM and Rosner MR . (2002). J. Biol. Chem., 277, 16733–16743.

  • Adams RH, Porras A, Alonso G, Jones M, Vintersten K, Panelli S, Valladares A, Perez L, Klein R and Nebreda AR . (2000). Mol. Cell., 6, 109–116.

  • Ahn NG, Seger R, Bratlien RL, Diltz CD, Tonks NK and Krebs EG . (1991). J. Biol. Chem., 266, 4220–4227.

  • Alberola-Ila J, Forbush KA, Seger R, Krebs EG and Perlmutter RM . (1995). Nature, 373, 620–623.

  • Alessi DR, Saito Y, Campbell DG, Cohen P, Sithanandam G, Rapp U, Ashworth A, Marshall CJ and Cowley S . (1994). EMBO J., 13, 1610–1619.

  • Aoki H, Kang PM, Hampe J, Yoshimura K, Noma T, Matsuzaki M and Izumo S . (2002). J. Biol. Chem., 277, 10244–10250.

  • Arbour N, Naniche D, Homann D, Davis RJ, Flavell RA and Oldstone MB . (2002). J. Exp. Med., 195, 801–810.

  • Balaban N, Moni J, Shannon M, Dang L, Murphy E and Goldkorn T . (1996). Biochim. Biophys. Acta, 1314, 147–156.

  • Behrens A, Sibilia M and Wagner EF . (1999). Nat. Genet., 21, 326–329.

  • Belanger LF, Roy S, Tremblay M, Brott B, Steff AM, Mourad W, Hugo P, Erikson R and Charron J . (2003). Mol. Cell. Biol., 23, 4778–4787.

  • Blaeser F, Ho N, Prywes R and Chatila TA . (2000). J. Biol. Chem., 275, 197–209.

  • Bohmann D, Bos TJ, Admon A, Nishimura T, Vogt PK and Tjian R . (1987). Science, 238, 1386–1392.

  • Bos JL . (1989). Cancer Res., 49, 4682–4689.

  • Boulton TG, Gregory JS, Jong SM, Wang LH, Ellis L and Cobb MH . (1990). J. Biol. Chem., 265, 2713–2719.

  • Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, Appella E and Fornace Jr AJ . (2001). Nature, 411, 102–107.

  • Caffrey DR, O'Neill LA and Shields DC . (1999). J. Mol. Evol., 49, 567–582.

  • Chang L and Karin M . (2001). Nature, 410, 37–40.

  • Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N, Munshi N, Kharbanda S and Anderson KC . (2003). J. Biol. Chem., 278, 17593–17596.

  • Chen S, Nguyen N, Tamura K, Karin M and Tukey RH . (2003). J. Biol. Chem., 278, 19526–19533.

  • Chen YR, Meyer CF and Tan TH . (1996). J. Biol. Chem., 271, 631–634.

  • Chen Z, Seimiya H, Naito M, Mashima T, Kizaki A, Dan S, Imaizumi M, Ichijo H, Miyazono K and Tsuruo T . (1999). Oncogene, 18, 173–180.

  • Coffer PJ, Burgering BM, Peppelenbosch MP, Bos JL and Kruijer W . (1995). Oncogene, 11, 561–569.

  • Coso OA, Chiariello M, Yu JC, Teramoto H, Crespo P, Xu N, Miki T and Gutkind JS . (1995). Cell, 81, 1137–1146.

  • Cowley S, Paterson H, Kemp P and Marshall CJ . (1994). Cell, 77, 841–852.

  • Crews CM, Alessandrini A and Erikson RL . (1992). Science, 258, 478–480.

  • Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S and Spiegel S . (1996). Nature, 381, 800–803.

  • Davis RJ . (1993). J. Biol. Chem., 268, 14553–14556.

  • Davis RJ . (2000). Cell, 103, 239–252.

  • Dent P, Yacoub A, Fisher PB, Hagan MP and Grant S . (2003). Oncogene, 22, 5885–5896.

  • Derijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M and Davis RJ . (1994). Cell, 76, 1025–1037.

  • Derijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ and Davis RJ . (1995). Science, 267, 682–685.

  • Dhanwada KR, Dickens M, Neades R, Davis R and Pelling JC . (1995). Oncogene, 11, 1947–1953.

  • Diehl NL, Enslen H, Fortner KA, Merritt C, Stetson N, Charland C, Flavell RA, Davis RJ and Rinç M . (2000). J. Exp. Med., 191, 321–334.

  • Dong C, Yang DD, Tournier C, Whitmarsh AJ, Xu J, Davis RJ and Flavell RA . (2000). Nature, 405, 91–94.

  • Dong C, Yang DD, Wysk M, Whitmarsh AJ, Davis RJ and Flavell RA . (1998). Science, 282, 2092–2095.

  • Dougherty CJ, Kubasiak LA, Prentice H, Andreka P, Bishopric NH and Webster KA . (2002). Biochem. J., 362, 561–571.

  • Eferl R, Ricci R, Kenner L, Zenz R, David JP, Rath M and Wagner EF . (2003). Cell, 112, 181–192.

  • English JM and Cobb MH . (2002). Trends. Pharmacol. Sci., 23, 40–45.

  • English JM, Vanderbilt CA, Xu S, Marcus S and Cobb MH . (1995). J. Biol. Chem., 270, 28897–28902.

  • Fields PE, Gajewski TF and Fitch FW . (1996). Science, 271, 1276–1278.

  • Fleming Y, Armstrong CG, Morrice N, Paterson A, Goedert M and Cohen P . (2000). Biochem. J., 352, 145–154.

  • Ganiatsas S, Kwee L, Fujiwara Y, Perkins A, Ikeda T, Labow MA and Zon LI . (1998). Proc. Natl. Acad. Sci. USA, 95, 6881–6886.

  • Gartner A, Nasmyth K and Ammerer G . (1992). Genes. Dev., 6, 1280–1292.

  • Ge B, Gram H, Di Padova F, Huang B, New L, Ulevitch RJ, Luo Y and Han J . (2002). Science, 295, 1291–1294.

  • Gille H, Kortenjann M, Thomae O, Moomaw C, Slaughter C, Cobb MH and Shaw PE . (1995). EMBO J., 14, 951–962.

  • Giroux S, Tremblay M, Bernard D, Cardin-Girard JF, Aubry S, Larouche L, Rousseau S, Huot J, Landry J, Jeannotte L and Charron J . (1999). Curr. Biol., 9, 369–372.

  • Guo Z, Clydesdale G, Cheng J, Kim K, Gan L, McConkey DJ, Ullrich SE, Zhuang Y and Su B . (2002). Mol. Cell. Biol., 22, 5761–5768.

  • Gupta S, Campbell D, Derijard B and Davis RJ . (1995). Science, 267, 389–393.

  • Han J, Jiang Y, Li Z, Kravchenko VV and Ulevitch RJ . (1997). Nature, 386, 296–299.

  • Han J, Lee JD, Bibbs L and Ulevitch RJ . (1994). Science, 265, 808–811.

  • Han J and Molkentin JD . (2000). Trends Cardiovasc. Med., 10, 19–22.

  • Hanahan D and Weinberg RA . (2000). Cell, 100, 57–70.

  • Hilberg F, Aguzzi A, Howells N and Wagner EF . (1993). Nature, 365, 179–181.

  • Hilger RA, Scheulen ME and Strumberg D . (2002). Onkologie, 25, 511–518.

  • Holbrook NJ, Liu Y and Fornace Jr AJ . (1996). Exs, 77, 273–288.

  • Holland PM, Suzanne M, Campbell JS, Noselli S and Cooper JA . (1997). J. Biol. Chem., 272, 24994–24998.

  • Huser M, Luckett J, Chiloeches A, Mercer K, Iwobi M, Giblett S, Sun XM, Brown J, Marais R and Pritchard C . (2001). EMBO J., 20, 1940–1951.

  • Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K and Gotoh Y . (1997). Science, 275, 90–94.

  • Irigoyen JP, Besser D and Nagamine Y . (1997). J. Biol. Chem., 272, 1904–1909.

  • Ito M, Yoshioka K, Akechi M, Yamashita S, Takamatsu N, Sugiyama K, Hibi M, Nakabeppu Y, Shiba T and Yamamoto KI . (1999). Mol. Cell. Biol., 19, 7539–7548.

  • Janknecht R, Ernst WH, Pingoud V and Nordheim A . (1993). EMBO J., 12, 5097–5104.

  • Johnson GL and Lapadat R . (2002). Science, 298, 1911–1912.

  • Johnson NL, Gardner AM, Diener KM, Lange-Carter CA, Gleavy J, Jarpe MB, Minden A, Karin M, Zon LI and Johnson GL . (1996). J. Biol. Chem., 271, 3229–3237.

  • Johnson RS, van Lingen B, Papaioannou VE and Spiegelman BM . (1993). Genes. Dev., 7, 1309–1317.

  • Juretic N, Santibanez JF, Hurtado C and Martinez J . (2001). J. Cell. Biochem., 83, 92–98.

  • Kamakura S, Moriguchi T and Nishida E . (1999). J. Biol. Chem., 274, 26563–26571.

  • Karin M . (1995). J. Biol. Chem., 270, 16483–16486.

  • Kato Y, Kravchenko VV, Tapping RI, Han J, Ulevitch RJ and Lee JD . (1997). EMBO J., 16, 7054–7066.

  • Kavanagh BD, Dent P, Schmidt-Ullrich RK, Chen P and Mikkelsen RB . (1998). Radiat. Res., 149, 579–587.

  • Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N, Pawson T, Woodgett JR and Iscove NN . (1996). EMBO J., 15, 7013–7025.

  • King KL and Cidlowski JA . (1995). J. Cell Biochem., 58, 175–180.

  • Kishimoto H, Nakagawa K, Watanabe T, Kitagawa D, Momose H, Seo J, Nishitai G, Shimizu N, Ohata S, Tanemura S, Asaka S, Goto T, Fukushi H, Yoshida H, Suzuki A, Sasaki T, Wada T, Penninger JM, Nishina H and Katada T . (2003). J. Biol. Chem., 278, 16595–16601.

  • Kitagawa D, Tanemura S, Ohta S, Shimizu N, Seo J, Nishitai G, Watanabe T, Nakagawa K, Kishimoto H, Wada T, Tezuka T, Yamamoto T, Nishina H and Katada T . (2002). J. Biol. Chem, 277, 366–371.

  • Kolodziejczyk SM, Wang L, Balazsi K, DeRepentigny Y, Kothary R and Megeney LA . (1999). Curr. Biol., 9, 1203–1206.

  • Konishi Y, Lehtinen M, Donovan N and Bonni A . (2002). Mol. Cell, 9, 1005–1016.

  • Kowenz-Leutz E, Twamley G, Ansieau S and Leutz A . (1994). Genes. Dev., 8, 2781–2791.

  • Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P and Flavell RA . (1999). Neuron, 22, 667–676.

  • Kyriakis JM and Avruch J . (2001). Physiol. Rev., 81, 807–869.

  • Lange-Carter CA, Pleiman CM, Gardner AM, Blumer KJ and Johnson GL . (1993). Science, 260, 315–319.

  • Latinis KM and Koretzky GA . (1996). Blood, 87, 871–875.

  • Laurent G and Jaffrezou JP . (2001). Blood, 98, 913–924.

  • Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R and Mikkelsen RB . (2001). Cancer Res., 61, 3894–3901.

  • Lee JD, Ulevitch RJ and Han J . (1995). Biochem. Biophys. Res. Commun., 213, 715–724.

  • Lee SH, Eom M, Lee SJ, Kim S, Park HJ and Park D . (2001). J. Biol. Chem., 276, 25066–25072.

  • Lenczowski JM, Dominguez L, Eder AM, King LB, Zacharchuk CM and Ashwell JD . (1997). Mol. Cell. Biol., 17, 170–181.

  • Lin A . (2003). Bioessays, 25, 17–24.

  • Lin Q, Schwarz J, Bucana C and Olson EN . (1997). Science, 276, 1404–1407.

  • Lin W, Kao HW, Robinson D, Kung HJ, Wu CW and Chen HC . (2000). Oncogene, 19, 5680–5689.

  • Li W, Whaley CD, Mondino A and Mueller DL . (1996). Science, 271, 1272–1276.

  • Lisovsky M, Itoh K and Sokol SY . (2002). Curr. Biol., 12, 53–58.

  • Liu B, Fang M, Lu Y, Mills GB and Fan Z . (2001). Br. J. Cancer, 85, 303–311.

  • Liu L, Cavanaugh JE, Wang Y, Sakagami H, Mao Z and Xia Z . (2003). Proc. Natl. Acad. Sci. USA, 100, 8532–8537.

  • Liu ZG, Hsu H, Goeddel DV and Karin M . (1996). Cell, 87, 565–576.

  • Liu ZG, Smith SW, McLaughlin KA, Schwartz LM and Osborne BA . (1994). Nature, 367, 281–284.

  • Lu HT, Yang DD, Wysk M, Gatti E, Mellman I, Davis RJ and Flavell RA . (1999). EMBO J., 18, 1845–1857.

  • Lu J, McKinsey TA, Nicol RL and Olson EN . (2000a). Proc. Natl. Acad. Sci. USA, 97, 4070–4075.

  • Lu J, McKinsey TA, Zhang CL and Olson EN . (2000b). Mol. Cell, 6, 233–244.

  • Lu X, Nemoto S and Lin A . (1997). J. Biol. Chem., 272, 24751–24754.

  • Mao Z, Bonni A, Xia F, Nadal-Vicens M and Greenberg ME . (1999). Science, 286, 785–790.

  • Mao Z and Wiedmann M . (1999). J. Biol. Chem., 274, 31102–31107.

  • Marais R, Wynne J and Treisman R . (1993). Cell, 73, 381–393.

  • Mathas S, Hinz M, Anagnostopoulos I, Krappmann D, Lietz A, Jundt F, Bommert K, Mechta-Grigoriou F, Stein H, Dorken B and Scheidereit C . (2002). EMBO J., 21, 4104–4113.

  • Maundrell K, Antonsson B, Magnenat E, Camps M, Muda M, Chabert C, Gillieron C, Boschert U, Vial-Knecht E, Martinou JC and Arkinstall S . (1997). J. Biol. Chem., 272, 25238–25242.

  • McDonald PH, Chow CW, Miller WE, Laporte SA, Field ME, Lin FT, Davis RJ and Lefkowitz RJ . (2000). Science, 290, 1574–1577.

  • McKinsey TA, Zhang CL and Olson EN . (2002). Trends. Biochem. Sci., 27, 40–47.

  • Mehta PB, Jenkins BL, McCarthy L, Thilak L, Robson CN, Neal DE and Leung HY . (2003). Oncogene, 22, 1381–1389.

  • Minden A, Lin A, McMahon M, Lange-Carter C, Derijard B, Davis RJ, Johnson GL and Karin M . (1994a). Science, 266, 1719–1723.

  • Minden A, Lin A, Smeal T, Derijard B, Cobb M, Davis R and Karin M . (1994b). Mol. Cell. Biol., 14, 6683–6688.

  • Mody N, Leitch J, Armstrong C, Dixon J and Cohen P . (2001). FEBS Lett., 502, 21–24.

  • Moriguchi T, Kawasaki H, Matsuda S, Gotoh Y and Nishida E . (1995). J. Biol. Chem., 270, 12969–12972.

  • Natoli G, Costanzo A, Ianni A, Templeton DJ, Woodgett JR, Balsano C and Levrero M . (1997). Science, 275, 200–203.

  • Naya FJ, Black BL, Wu H, Bassel-Duby R, Richardson JA, Hill JA and Olson EN . (2002). Nat. Med., 8, 1303–1309.

  • Nishina H, Fischer KD, Radvanyi L, Shahinian A, Hakem R, Rubie EA, Bernstein A, Mak TW, Woodgett JR and Penninger JM . (1997). Nature, 385, 350–353.

  • Nishina H, Vaz C, Billia P, Nghiem M, Sasaki T, De la Pompa JL, Furlonger K, Paige C, Hui C, Fischer KD, Kishimoto H, Iwatsubo T, Katada T, Woodgett JR and Penninger JM . (1999). Development, 126, 505–516.

  • Nishitai G, Shimizu N, Negishi T, Kishimoto H, Nakagawa K, Kitagawa D, Watanabe T, Momose H, Ohata S, Tanemura S, Asaka S, Kubota J, Saito R, Yoshida H, Mak TW, Wada T, Penninger JM, Azuma N, Nishina H and Katada T . (2003). J. Biol. Chem., 279, 1621–1626.

  • Okamoto S, Krainc D, Sherman K and Lipton SA . (2000). Proc. Natl. Acad. Sci. USA, 97, 7561–7566.

  • Olson MF, Ashworth A and Hall A . (1995). Science, 269, 1270–1272.

  • Pages G, Guerin S, Grall D, Bonino F, Smith A, Anjuere F, Auberger P and Pouyssegur J . (1999). Science, 286, 1374–1377.

  • Park JM, Greten FR, Li ZW and Karin M . (2002). Science, 297, 2048–2051.

  • Pearson G, English JM, White MA and Cobb MH . (2001). J. Biol. Chem., 276, 7927–7931.

  • Platanias LC . (2003). Blood, 101, 4667–4679.

  • Porras A, Zuluaga S, Black E, Valladares A, Alvarez AM, Ambrosino C, Benito M and Nebreda AR . (2004). Mol Biol Cell, 15, 922–933.

  • Prasad MV, Dermott JM, Heasley LE, Johnson GL and Dhanasekaran N . (1995). J. Biol. Chem., 270, 18655–18659.

  • Price MA, Cruzalegui FH and Treisman R . (1996). EMBO J., 15, 6552–6563.

  • Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ and Davis RJ . (1995). J. Biol. Chem., 270, 7420–7426.

  • Regan CP, Li W, Boucher DM, Spatz S, Su MS and Kuida K . (2002). Proc. Natl. Acad. Sci. USA, 99, 9248–9253.

  • Robinson D, He F, Pretlow T and Kung HJ . (1996). Proc. Natl. Acad. Sci. USA, 93, 5958–5962.

  • Rodrigues GA, Park M and Schlessinger J . (1997). EMBO J., 16, 2634–2645.

  • Rowinsky EK, Windle JJ and Von Hoff DD . (1999). J. Clin. Oncol., 17, 3631–3652.

  • Sabapathy K, Hu Y, Kallunki T, Schreiber M, David JP, Jochum W, Wagner EF and Karin M . (1999). Curr. Biol., 9, 116–125.

  • Sabapathy K, Kallunki T, David JP, Graef I, Karin M and Wagner EF . (2001). J. Exp. Med., 193, 317–328.

  • Sadoshima J, Montagne O, Wang Q, Yang G, Warden J, Liu J, Takagi G, Karoor V, Hong C, Johnson GL, Vatner DE and Vatner SF . (2002). J. Clin. Invest., 110, 271–279.

  • Salmon RA, Foltz IN, Young PR and Schrader JW . (1997). J. Immunol., 159, 5309–5317.

  • Sanchez I, Hughes RT, Mayer BJ, Yee K, Woodgett JR, Avruch J, Kyriakis JM and Zon LI . (1994). Nature, 372, 794–798.

  • Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Valerie K, Dent P and Fisher PB . (2002). Proc. Natl. Acad. Sci. USA, 99, 10054–10059.

  • Sasaki T, Wada T, Kishimoto H, Irie-Sasaki J, Matsumoto G, Goto T, Yao Z, Wakeham A, Mak TW, Suzuki A, Cho SK, Zuniga-Pflucker JC, Oliveira-dos-Santos AJ, Katada T, Nishina H and Penninger JM . (2001). J. Exp. Med., 194, 757–768.

  • Schmidt-Ullrich RK, Mikkelsen RB, Dent P, Todd DG, Valerie K, Kavanagh BD, Contessa JN, Rorrer WK and Chen PB . (1997). Oncogene, 15, 1191–1197.

  • Schreiber M, Kolbus A, Piu F, Szabowski A, Mohle-Steinlein U, Tian J, Karin M, Angel P and Wagner EF . (1999). Genes Dev., 13, 607–619.

  • Sebolt-Leopold JS . (2000). Oncogene, 19, 6594–6599.

  • Seger R and Krebs EG . (1995). FASEB J., 9, 726–735.

  • Seimiya H, Mashima T, Toho M and Tsuruo T . (1997). J. Biol. Chem., 272, 4631–4636.

  • Shaulian E, Schreiber M, Piu F, Beeche M, Wagner EF and Karin M . (2000). Cell, 103, 897–907.

  • Shi Y, Kotlyarov A, Laabeta K, Gruber AD, Butt E, Marcus K, Meyer HE, Friedrich A, Volk HD and Gaestel M . (2003). Mol. Cell. Biol., 23, 7732–7741.

  • Sohn SJ, Sarvis BK, Cado D and Winoto A . (2002). J. Biol. Chem., 277, 43344–43351.

  • Stadheim TA and Kucera GL . (2002). Leuk. Res., 26, 55–65.

  • Sturgill TW, Ray LB, Erikson E and Maller JL . (1988). Nature, 334, 715–718.

  • Su B, Jacinto E, Hibi M, Kallunki T, Karin M and Ben-Neriah Y . (1994). Cell, 77, 727–736.

  • Su B and Karin M . (1996). Curr. Opin. Immunol., 8, 402–411.

  • Su GH, Song JJ, Repasky EA, Schutte M and Kern SE . (2002). Hum. Mutat., 19, 81.

  • Suzaki Y, Yoshizumi M, Kagami S, Koyama AH, Taketani Y, Houchi H, Tsuchiya K, Takeda E and Tamaki T . (2002). J. Biol. Chem., 277, 9614–9621.

  • Swat W, Fujikawa K, Ganiatsas S, Yang D, Xavier RJ, Harris NL, Davidson L, Ferrini R, Davis RJ, Labow MA, Flavell RA, Zon LI and Alt FW . (1998). Immunity, 8, 625–634.

  • Takeda K, Matsuzawa A, Nishitoh H and Ichijo H . (2003). Cell. Struct. Funct., 28, 23–29.

  • Takenaka K, Moriguchi T and Nishida E . (1998). Science, 280, 599–602.

  • Tamura K, Sudo T, Senftleben U, Dadak AM, Johnson R and Karin M . (2000). Cell, 102, 221–231.

  • Tanaka N, Kamanaka M, Enslen H, Dong C, Wysk M, Davis RJ and Flavell RA . (2002). EMBO Rep., 3, 785–791.

  • Teng DH, Perry III WL, Hogan JK, Baumgard M, Bell R, Berry S, Davis T, Frank D, Frye C, Hattier T, Hu R, Jammulapati S, Janecki T, Leavitt A, Mitchell JT, Pero R, Sexton D, Schroeder M, Su PH, Swedlund B, Kyriakis JM, Avruch J, Bartel P, Wong AK and Tavtigian SV . (1997). Cancer Res., 57, 4177–4182.

  • Tibbles LA, Ing YL, Kiefer F, Chan J, Iscove N, Woodgett JR and Lassam NJ . (1996). EMBO J., 15, 7026–7035.

  • Tibbles LA and Woodgett JR . (1999). Cell. Mol. Life Sci., 55, 1230–1254.

  • Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T and Ichijo H . (2001). EMBO Rep., 2, 222–228.

  • Tournier C, Dong C, Turner TK, Jones SN, Flavell RA and Davis RJ . (2001). Genes Dev., 15, 1419–1426.

  • Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA and Davis RJ . (2000). Science, 288, 870–874.

  • Tournier C, Whitmarsh AJ, Cavanagh J, Barrett T and Davis RJ . (1997). Proc. Natl. Acad. Sci. USA, 94, 7337–7342.

  • Treisman R . (1996). Curr. Opin. Cell. Biol., 8, 205–215.

  • Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM, Haimovitz-Friedman A, Fuks Z and Kolesnick RN . (1996). Nature, 380, 75–79.

  • Wada T, Joza N, Cheng H-YM, Sasaki T, Kozieradzki I, Bachmaier K, Katada T, Schreiber M, Wagner EF, Nishina H and Penninger JM . (2004). Nat. Cell. Biol., 6, 215–226.

  • Wada T, Nakagawa K, Watanabe T, Nishitai G, Seo J, Kishimoto H, Kitagawa D, Sasaki T, Penninger JM, Nishina H and Katada T . (2001). J. Biol. Chem., 276, 30892–30897.

  • Wadman IA, Hsu HL, Cobb MH and Baer R . (1994). Oncogene, 9, 3713–3716.

  • Wang X, Xu L, Wang H, Young PR, Gaestel M and Feuerstein GZ . (2002). J. Biol. Chem., 277, 43968–43972.

  • Waskiewicz AJ and Cooper JA . (1995). Curr. Opin. Cell. Biol., 7, 798–805.

  • Watanabe T, Nakagawa K, Ohata S, Kitagawa D, Nishitai G, Seo J, Tanemura S, Shimizu N, Kishimoto H, Wada T, Aoki J, Arai H, Iwatsubo T, Mochita M, Satake M, Ito Y, Matsuyama T, Mak TW, Penninger JM, Nishina H and Katada T . (2002). Dev. Biol., 250, 332–347.

  • Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ and Segal RA . (2001). Nat. Neurosci., 4, 981–988.

  • Weldon CB, Scandurro AB, Rolfe KW, Clayton JL, Elliott S, Butler NN, Melnik LI, Alam J, McLachlan JA, Jaffe BM, Beckman BS and Burow ME . (2002). Surgery, 132, 293–301.

  • Werlen G, Hausmann B, Naeher D and Palmer E . (2003). Science, 299, 1859–1863.

  • Westwick JK, Bielawska AE, Dbaibo G, Hannun YA and Brenner DA . (1995). J. Biol. Chem., 270, 22689–22692.

  • Whitmarsh AJ, Cavanagh J, Tournier C, Yasuda J and Davis RJ . (1998). Science, 281, 1671–1674.

  • Widmann C, Gibson S, Jarpe MB and Johnson GL . (1999). Physiol. Rev., 79, 143–180.

  • Williams N . (1996). Science, 271, 1234.

  • Wilson DJ, Fortner KA, Lynch DH, Mattingly RR, Macara IG, Posada JA and Budd RC . (1996). Eur. J. Immunol., 26, 989–994.

  • Woodgett JR, Avruch J and Kyriakis J . (1996). Cancer Surv., 27, 127–138.

  • Woronicz JD, Calnan B, Ngo V and Winoto A . (1994). Nature, 367, 277–281.

  • Xia Z, Dickens M, Raingeaud J, Davis RJ and Greenberg ME . (1995). Science, 270, 1326–1331.

  • Yamamoto K, Ichijo H and Korsmeyer SJ . (1999). Mol. Cell. Biol., 19, 8469–8478.

  • Yan M, Dai T, Deak JC, Kyriakis JM, Zon LI, Woodgett JR and Templeton DJ . (1994). Nature, 372, 798–800.

  • Yang DD, Conze D, Whitmarsh AJ, Barrett T, Davis RJ, Rincon M and Flavell RA . (1998). Immunity, 9, 575–585.

  • Yang DD, Kuan CY, Whitmarsh AJ, Rincon M, Zheng TS, Davis RJ, Rakic P and Flavell RA . (1997). Nature, 389, 865–870.

  • Yosimichi G, Nakanishi T, Nishida T, Hattori T, Takano-Yamamoto T and Takigawa M . (2001). Eur. J. Biochem., 268, 6058–6065.

  • Youn HD, Chatila TA and Liu JO . (2000). EMBO J., 19, 4323–4331.

  • Yujiri T, Sather S, Fanger GR and Johnson GL . (1998). Science, 282, 1911–1914.

  • Yu R, Shtil AA, Tan TH, Roninson IB and Kong AN . (1996). Cancer Lett., 107, 73–81.

  • Zanke BW, Boudreau K, Rubie E, Winnett E, Tibbles LA, Zon L, Kyriakis J, Liu FF and Woodgett JR . (1996). Curr. Biol., 6, 606–613.

  • Zetser A, Gredinger E and Bengal E . (1999). J. Biol. Chem., 274, 5193–5200.

  • Zhang J, Gao JX, Salojin K, Shao Q, Grattan M, Meagher C, Laird DW and Delovitch TL . (2000). J. Exp. Med., 191, 1017–1030.

  • Zhou G, Bao ZQ and Dixon JE . (1995). J. Biol. Chem., 270, 12665–12669.

Download references

Author information

Authors and Affiliations

  1. IMBA: Institute of Molecular Biotechnology of the Austrian Academy of Sciences, Dr Bohr-gasse3–5, Vienna, A-1030, Austria

    Teiji Wada & Josef M Penninger

Authors
  1. Teiji Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Josef M Penninger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Josef M Penninger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wada, T., Penninger, J. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838–2849 (2004). https://doi.org/10.1038/sj.onc.1207556

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1207556

Keywords

This article is cited by

Search

Advanced search

Quick links