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Pflügers Archiv - European Journal of Physiology

, Volume 458, Issue 5, pp 953–967 | Cite as

The mammalian family of sterile 20p-like protein kinases

  • Eric Delpire
Signaling and Cell Physiology

Abstract

Twenty-eight kinases found in mammalian genomes share similarity to the budding yeast kinase Ste20p. This review article examines the biological function of these mammalian Ste20 kinases. Some of them have conserved the Ste20p function of transducing extracellular signals to mitogen-activated kinases. Others affect ion transport, cell cycle, cytoskeleton organization, and program cell death. A number of molecular details involved in the activation of the kinases are discussed including autophosphorylation, substrate recognition, autoinhibition, dimerization, and substrate binding.

Keywords

Chloride transport Cell volume Cell cycle Cytoskeleton Protein kinase Signal transduction 

Abbreviations

CHK

Checkpoint kinase

ClC

Chloride channel, ClC family

DAPK

Death associated protein kinase

EGF

Epidermal growth factor

ERK

Extracellular signal-regulated kinase

GCK

Germinal center kinase

GCKR

GCK-related

GBP3

Guanylate binding protein 3

GLK

GCK-like kinase

HPK1

Hematopoietic progenitor kinase 1

JIK

JNK inhibitory kinase

JNK

c-jun N-terminal kinase

KCC

K-Cl cotransporter

KFC

Kinase from chicken

KHS

Kinase homologous to SPS1/Ste20

KRS

Kinase responsive to stress

LIMK

LIM motif-containing kinase

LOK

Lymphocyte oriented kinase

LOSK

Long Ste20-like kinase

MAPK

Mitogen-activated kinase

MAP2K

Mitogen-activated kinase kinase

MAP3K

Mitogen-activated kinase kinase kinase

MAP4K

Mitogen-activated kinase kinase kinase kinase

MASK

Mst3 and SOK1-related kinase

MEK

Kinase

MEKK

Kinase kinase

Mink

Mishappen/NIK-related kinase

Mst

Mammalian sterile 20

NESK

Nck-interacting kinase-like embryo-specific kinase

NIK

Nck-interacting kinase

NKCC

Na-K-2Cl cotransporter

NRK

NIK-related kinase

OSR

Oxidative stress response

PAK

p21-activated kinase

PDGF

Platelet-derived growth factor

PKA

Protein kinase A

PKC

Protein kinase C

PASK

Proline alanine rich Ste20 kinase

PSK

Prostate-derived Ste20 kinase

SLK

Synthetic lethal kinase

SPAK

Ste20-related proline alanine rich kinase

Ste

Sterile

S/T

Serine/threonine kinases

TAO

Thousand and one, as for the thousand and one amino acid of TAO1

TNIK

Traf and Nck-interacting kinase

TNF

Tumor necrosis factor

TRAF

TNF receptor-associated factor

WNK

With no lysine kinase

Notes

Acknowledgements

Work on Ste20 kinases in the author’s laboratory is supported by NIH grant GM74771.

References

  1. 1.
    Abo A, Qu J, Cammarano MS et al (1998) PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J 17:6527–6540PubMedCrossRefGoogle Scholar
  2. 2.
    Adams JA (2001) Kinetic and catalytic mechanisms of protein kinases. Chem Rev 101:2271–2290PubMedCrossRefGoogle Scholar
  3. 3.
    Allen KM, Gleeson JG, Bagrodia S et al (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat Genet 20:25–30PubMedCrossRefGoogle Scholar
  4. 4.
    Anand R, Kim AY, Brent M et al (2008) Biochemical analysis of MST1 kinase: elucidation of a C-terminal regulatory region. Biochemistry 42:6719–6726CrossRefGoogle Scholar
  5. 5.
    Asrar S, Meng Y, Zhou Z et al (2008) Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1). Neuropharmacology 56:73–80PubMedCrossRefGoogle Scholar
  6. 6.
    Berman KS, Hutchison M, Avery L et al (2001) kin-18, a C. elegans protein kinase involved in feeding. Gene 279:137–147PubMedCrossRefGoogle Scholar
  7. 7.
    Bienvenu T, des Portes V, McDonell N et al (2000) Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am J Med Genet 93:294–298PubMedCrossRefGoogle Scholar
  8. 8.
    Bokoch GM (2003) Biology of the p21-activated kinases. Annu Rev Biochem 72:743–781PubMedCrossRefGoogle Scholar
  9. 9.
    Burakov AV, Zhapparova ON, Kovalenko OV et al (2008) Ste20-related protein kinase LOSK (SLK) controls microtubule radial array in interphase. Mol Biol Cell 19:1952–1961PubMedCrossRefGoogle Scholar
  10. 10.
    Chaar Z, O’Reilly P, Gelman I et al (2006) v-Src-dependent down-regulation of the Ste20-like kinase SLK by casein kinase II. J Biol Chem 281:28193–28199PubMedCrossRefGoogle Scholar
  11. 11.
    Chadee DN, Yuasa T, Kyriakis JM (2002) Direct activation of mitogen-activated protein kinase kinase kinase MEKK1 by the Ste20p homologue GCK and the adapter protein TRAF2. Mol Cell Biol 22:737–749PubMedCrossRefGoogle Scholar
  12. 12.
    Chen Z, Hutchison M, Cobb MH (1999) Isolation of the protein kinase TAO2 and identification of its mitogen-activated protein kinase/extracellular signal-regulated kinase kinase binding domain. J Biol Chem 274:28803–28807PubMedCrossRefGoogle Scholar
  13. 13.
    Ching YP, Leong VY, Wong CM et al (2003) Identification of an autoinhibitory domain of p21-activated protein kinase 5. J Biol Chem 278:33621–33624PubMedCrossRefGoogle Scholar
  14. 14.
    Choe KP, Strange K (2007) Evolutionarily conserved WNK and Ste20 kinases are essential for acute volume recovery and survival after hypertonic shrinkage in Caenorhabditis elegans. Am J Physiol Cell Physiol 293:C915–C927PubMedCrossRefGoogle Scholar
  15. 15.
    Choe KP, Lamitina T, Strange K (2006) GCK-3, a Caenorhabditis elegans homologue of PASK, is essential for whole-animal osmotic homeostasis. FASEB J 20:A838CrossRefGoogle Scholar
  16. 16.
    Conder R, Yu H, Ricos M et al (2004) dPak is required for integrity of the leading edge cytoskeleton during Drosophila dorsal closure but does not signal through the JNK cascade. Dev Biol 276:378–390PubMedCrossRefGoogle Scholar
  17. 17.
    Creasy CL, Chernoff J (1995) Cloning and characterization of a human protein kinase with homology to Ste20. J Biol Chem 270:21695–21700PubMedCrossRefGoogle Scholar
  18. 18.
    Creasy CL, Chernoff J (1995) Cloning and characterization of a member of the MST subfamily of Ste20-like kinases. Gene 167:303–306PubMedCrossRefGoogle Scholar
  19. 19.
    Creasy CL, Ambrose DM, Chernoff J (1996) The Ste20-like protein kinase, Mst1, dimerizes and contains an inhibitory domain. J Biol Chem 271:21049–21053PubMedCrossRefGoogle Scholar
  20. 20.
    Dan I, Watanabe NM, Kobayashi T et al (2000) Molecular cloning of MINK, a novel member of mammalian GCK family kinases, which is up-regulated during postnatal mouse cerebral development. FEBS Lett 469:19–23PubMedCrossRefGoogle Scholar
  21. 21.
    Dan I, Watanabe NM, Kusumi A (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11:220–230PubMedCrossRefGoogle Scholar
  22. 22.
    Dan C, Nath N, Liberto M et al (2002) PAK5, a new brain-specific kinase, promotes neurite outgrowth in N1E–115 cells. Mol Cell Biol 22:567–577PubMedCrossRefGoogle Scholar
  23. 23.
    Dan I, Ong SE, Watanabe NM et al (2002) Cloning of MASK, a novel member of the mammalian germinal center kinase III subfamily, with apoptosis-inducing properties. J Biol Chem 277:5929–5939PubMedCrossRefGoogle Scholar
  24. 24.
    Delpire E, Gagnon KB (2006) SPAK and OSR1, key kinases involved in the regulation of chloride transport. Acta Physiol (Oxf) 187:103–113CrossRefGoogle Scholar
  25. 25.
    Delpire E, Gagnon KB (2007) Genome-wide analysis of SPAK/OSR1 binding motifs. Physiol Genomics 28:223–231PubMedGoogle Scholar
  26. 26.
    Delpire E, Gagnon KB (2008) SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J 409:321–331PubMedCrossRefGoogle Scholar
  27. 27.
    Delpire E, Piechotta K (2004) Ste20 kinases and cation-chloride cotransporters. In: Lauf PK, Adragna NC (eds) Cell volume and signaling, vol 559, Advances in experimental medicine and biology. Springer, Heidelberg, pp 43–53CrossRefGoogle Scholar
  28. 28.
    Denton J, Nehrke K, Yin X et al (2005) GCK-3, a newly identified Ste20 kinase, binds to and regulates the activity of a cell cycle-dependent ClC anion channel. J Gen Physiol 125:113–125PubMedCrossRefGoogle Scholar
  29. 29.
    Dose AC, Burnside B (2000) Cloning and chromosomal localization of a human class III myosin. Genomics 67:333–342PubMedCrossRefGoogle Scholar
  30. 30.
    Dose AC, Burnside B (2002) A class III myosin expressed in the retina is a potential candidate for Bardet–Biedl syndrome. Genomics 79:621–624PubMedCrossRefGoogle Scholar
  31. 31.
    Dose AC, Hillman DW, Wong C et al (2003) Myo3A, one of two class III myosin genes expressed in vertebrate retina, is localized to the calycal processes of rod and cone photoreceptors and is expressed in the sacculus. Mol Biol Cell 14:1058–1073PubMedCrossRefGoogle Scholar
  32. 32.
    Dose AC, Ananthanarayanan S, Moore JE et al (2008) The kinase domain alters the kinetic properties of the myosin IIIA motor. Biochemistry 47:2485–2496PubMedCrossRefGoogle Scholar
  33. 33.
    Dowd BF, Forbush B (2003) PASK (proline-alanine-rich Ste20-related kinase), a regulatory kinase of the Na-K-Cl cotransporter (NKCC1). J Biol Chem 278:27347–27353PubMedCrossRefGoogle Scholar
  34. 34.
    Draviam VM, Stegmeier F, Nalepa G et al (2007) A functional genomic screen identifies a role for TAO1 kinase in spindle-checkpoint signalling. Nat Cell Biol 9:556–564PubMedCrossRefGoogle Scholar
  35. 35.
    Endo J, Toyama-Sorimachi N, Taya C et al (2000) Deficiency of a STE20/PAK family kinase LOK leads to the acceleration of LFA-1 clustering and cell adhesion of activated lymphocytes. FEBS Lett 468:234–238PubMedCrossRefGoogle Scholar
  36. 36.
    Falin RA, Morrison R, Ham AJ et al (2009) Identification of regulatory phosphorylation sites in a cell volume- and Ste20 kinase-dependent ClC anion channel. J Gen Physiol 133:29–42PubMedCrossRefGoogle Scholar
  37. 37.
    Findlay GM, Yan L, Procter J et al (2007) A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. Biochem J 403:13–20PubMedCrossRefGoogle Scholar
  38. 38.
    Fu CA, Shen M, Huang BC et al (1999) TNIK, a novel member of the germinal center kinase family that activates the c-Jun N-terminal kinase pathway and regulates the cytoskeleton. J Biol Chem 274:30729–30737PubMedCrossRefGoogle Scholar
  39. 39.
    Gagnon KB, England R, Delpire E (2006) Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol Cell Biol 26:689–698PubMedCrossRefGoogle Scholar
  40. 40.
    Gagnon KB, England R, Delpire E (2006) Volume sensitivity of cation-chloride cotransporters is modulated by the interaction of two kinases: SPAK and WNK4. Am J Physiol Cell Physiol 290:C134–C142PubMedCrossRefGoogle Scholar
  41. 41.
    Gagnon KB, England R, Delpire E (2007) A single binding motif is required for SPAK activation of the Na-K-2Cl cotransporter. Cell Physiol Biochem 20:131–142PubMedGoogle Scholar
  42. 42.
    Gedeon AK, Nelson J, Gecz J et al (2003) X-linked mild non-syndromic mental retardation with neuropsychiatric problems and the missense mutation A365E in PAK3. Am J Med Genet A 120A:509–517PubMedCrossRefGoogle Scholar
  43. 43.
    Glantschnig H, Rodan GA, Reszka AA (2002) Mapping of MST1 kinase sites of phosphorylation. Activation and autophosphorylation. J Biol Chem 277:42987–42996PubMedCrossRefGoogle Scholar
  44. 44.
    Graves JD, Gotoh Y, Draves KE et al (1998) Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J 17:2224–2234PubMedCrossRefGoogle Scholar
  45. 45.
    Graves JD, Draves KE, Gotoh Y et al (2001) Both phosphorylation and caspase-mediated cleavage contribute to regulation of the Ste20-like protein kinase Mst1 during CD95/Fas-induced apoptosis. J Biol Chem 276:14909–14915PubMedCrossRefGoogle Scholar
  46. 46.
    Gu Y, Luo T, Yang J et al (2006) The -822G/A polymorphism in the promoter region of the MAP4K5 gene is associated with reduced risk of type 2 diabetes in Chinese Hans from Shanghai. J Hum Genet 51:605–610PubMedCrossRefGoogle Scholar
  47. 47.
    Hao W, Takano T, Guillemette J et al (2006) Induction of apoptosis by the Ste20-like kinase SLK, a germinal center kinase that activates apoptosis signal-regulating kinase and p38. J Biol Chem 281:3075–3084PubMedCrossRefGoogle Scholar
  48. 48.
    Hipfner DR, Cohen SM (2003) The Drosophila sterile-20 kinase slik controls cell proliferation and apoptosis during imaginal disc development. PLoS Biol 1:E35PubMedCrossRefGoogle Scholar
  49. 49.
    Hu MC, Qiu WR, Wang X et al (1996) Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev 10:2251–2264PubMedCrossRefGoogle Scholar
  50. 50.
    Huang CY, Wu YM, Hsu CY et al (2002) Caspase activation of mammalian sterile 20-like kinase 3 (Mst3). Nuclear translocation and induction of apoptosis. J Biol Chem 277:34367–34374PubMedCrossRefGoogle Scholar
  51. 51.
    Hutchison M, Berman KS, Cobb MH (1998) Isolation of TAO1, a protein kinase that activates MEKs in stress-activated protein kinase cascades. J Biol Chem 273:28625–28632PubMedCrossRefGoogle Scholar
  52. 52.
    Jaffer ZM, Chernoff J (2002) p21-activated kinases: three more join the Pak. Int J Biochem Cell Biol 34:713–717PubMedCrossRefGoogle Scholar
  53. 53.
    Jakobi R, Chen CJ, Tuazon PT et al (1996) Molecular cloning and sequencing of the cytostatic G protein-activated protein kinase PAK I. J Biol Chem 271:6206–6211PubMedCrossRefGoogle Scholar
  54. 54.
    Katz P, Whalen G, Kehrl JH (1994) Differential expression of a novel protein kinase in human B lymphocytes. Preferential localization in the germinal center. J Biol Chem 269:16802–16809PubMedGoogle Scholar
  55. 55.
    Kiger AA, Baum B, Jones S et al (2003) A functional genomic analysis of cell morphology using RNA interference. J Biol 2:27PubMedCrossRefGoogle Scholar
  56. 56.
    Koeppel MA, McCarthy CC, Moertl E et al (2004) Identification and characterization of PS-GAP as a novel regulator of caspase-activated PAK-2. J Biol Chem 279:53653–53664PubMedCrossRefGoogle Scholar
  57. 57.
    Komaba S, Inoue A, Maruta S et al (2003) Determination of human myosin III as a motor protein having a protein kinase activity. J Biol Chem 278:21352–21360PubMedCrossRefGoogle Scholar
  58. 58.
    Kumar R, Gururaj AE, Barnes CJ (2006) p21-activated kinases in cancer. Nat Rev Cancer 6:459–471PubMedCrossRefGoogle Scholar
  59. 59.
    Kuramochi S, Moriguchi T, Kuida K et al (1997) LOK is a novel mouse STE20-like protein kinase that is expressed predominantly in lymphocytes. J Biol Chem 272:22679–22684PubMedCrossRefGoogle Scholar
  60. 60.
    Lee SJ, Montell C (2004) Light-dependent translocation of visual arrestin regulated by the NINAC myosin III. Neuron 43:95–103PubMedCrossRefGoogle Scholar
  61. 61.
    Lee WS, Hsu CY, Wang PL et al (2004) Identification and characterization of the nuclear import and export signals of the mammalian Ste20-like protein kinase 3. FEBS Lett 572:41–45PubMedCrossRefGoogle Scholar
  62. 62.
    Lee SJ, Cobb MH, Goldsmith EJ (2009) Crystal structure of domain-swapped STE20 OSR1 kinase domain. Protein Sci 18:304–313PubMedCrossRefGoogle Scholar
  63. 63.
    Lehtinen MK, Yuan Z, Boag PR et al (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987–1001PubMedCrossRefGoogle Scholar
  64. 64.
    Lei M, Lu W, Meng W et al (2000) Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102:387–397PubMedCrossRefGoogle Scholar
  65. 65.
    Leiserson WM, Harkins EW, Keshishian H (2000) Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheatment. Neuron 28:793–806PubMedCrossRefGoogle Scholar
  66. 66.
    Li X, Minden A (2003) Targeted disruption of the gene for the PAK5 kinase in mice. Mol Cell Biol 23:7134–7142PubMedCrossRefGoogle Scholar
  67. 67.
    Lin JL, Chen HC, Fang HI et al (2001) MST4, a new Ste20-related kinase that mediates cell growth and transformation via modulating ERK pathway. Oncogene 20:6559–6569PubMedCrossRefGoogle Scholar
  68. 68.
    Ling P, Lu TJ, Yuan CJ et al (2008) Biosignaling of mammalian Ste20-related kinases. Cell Signal 20:1237–1247PubMedCrossRefGoogle Scholar
  69. 69.
    Lu TJ, Lai WY, Huang CY et al (2006) Inhibition of cell migration by autophosphorylated mammalian sterile 20-like kinase 3 (MST3) involves paxillin and protein-tyrosine phosphatase-PEST. J Biol Chem 281:38405–38417PubMedCrossRefGoogle Scholar
  70. 70.
    Ma X, Zhao H, Shan J et al (2007) PDCD10 interacts with Ste20-related kinase MST4 to promote cell growth and transformation via modulation of the ERK pathway. Mol Biol Cell 18:1965–1978PubMedCrossRefGoogle Scholar
  71. 71.
    Machida N, Umikawa M, Takei K et al (2004) Mitogen-activated protein kinase kinase kinase kinase 4 as a putative effector of Rap2 to activate the c-Jun N-terminal kinase. J Biol Chem 279:15711–15714PubMedCrossRefGoogle Scholar
  72. 72.
    Manser E, Chong C, Zhao ZS et al (1995) Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) family. J Biol Chem 270:25070–25070PubMedCrossRefGoogle Scholar
  73. 73.
    Martin GA, Bollag G, McCormick F et al (1995) A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J 14:1970–1978PubMedGoogle Scholar
  74. 74.
    Matsui Y, Nakano N, Shao D et al (2008) Lats2 is a negative regulator of myocyte size in the heart. Circ Res 103:1309–1318PubMedCrossRefGoogle Scholar
  75. 75.
    Melzig J, Rein KH, Schafer U et al (1998) A protein related to p21-activated kinase (PAK) that is involved in neurogenesis in the Drosophila adult central nervous system. Curr Biol 8:1223–1226PubMedCrossRefGoogle Scholar
  76. 76.
    Mitsopoulos C, Zihni C, Garg R et al (2003) The prostate-derived sterile 20-like kinase (PSK) regulates microtubule organization and stability. J Biol Chem 278:18085–18091PubMedCrossRefGoogle Scholar
  77. 77.
    Moriguchi T, Urushiyama S, Hisamoto N et al (2006) WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related kinases, SPAK and OSR1. J Biol Chem 280:42685–42693CrossRefGoogle Scholar
  78. 78.
    Nakano K, Yamauchi J, Nakagawa K et al (2000) NESK, a member of the germinal center kinase family that activates the c-Jun N-terminal kinase pathway and is expressed during the late stages of embryogenesis. J Biol Chem 275:20533–20539PubMedCrossRefGoogle Scholar
  79. 79.
    Nekrasova T, Jobes ML, Ting JH et al (2008) Targeted disruption of the Pak5 and Pak6 genes in mice leads to deficits in learning and locomotion. Dev Biol 322:95–108PubMedCrossRefGoogle Scholar
  80. 80.
    Nolen B, Taylor S, Ghosh G (2004) Regulation of protein kinases: controlling activity through activation segment conformation. Mol Cell 15:661–675PubMedCrossRefGoogle Scholar
  81. 81.
    Peippo M, Koivisto AM, Sarkamo T et al (2007) PAK3 related mental disability: further characterization of the phenotype. Am J Med Genet A 143A:2406–2016PubMedCrossRefGoogle Scholar
  82. 82.
    Piechotta K, Lu J, Delpire E (2002) Cation-chloride cotransporters interact with the stress-related kinases SPAK and OSR1. J Biol Chem 277:50812–50819PubMedCrossRefGoogle Scholar
  83. 83.
    Piechotta K, Garbarini NJ, England R et al (2003) Characterization of the interaction of the stress kinase SPAK with the Na+-K+-2Cl- cotransporter in the nervous system: evidence for a scaffolding role of the kinase. J Biol Chem 278:52848–52856PubMedCrossRefGoogle Scholar
  84. 84.
    Pike AC, Rellos P, Niesen FH et al (2008) Activation segment dimerization: a mechanism for kinase autophosphorylation of non-consensus sites. EMBO J 27:704–714PubMedCrossRefGoogle Scholar
  85. 85.
    Poinat P, De Arcangelis A, Sookhareea S et al (2002) A conserved interaction between beta1 integrin/PAT-3 and Nck-interacting kinase/MIG-15 that mediates commissural axon navigation in C. elegans. Curr Biol 12:622–631PubMedCrossRefGoogle Scholar
  86. 86.
    Pombo CM, Bonventre JV, Molnar A et al (1996) Activation of a human Ste-20-like kinase by oxidant stress defines a novel stress response pathway. EMBO J 15:5437–4546Google Scholar
  87. 87.
    Ponce-Coria J, San-Cristobal P, Kahle KT et al (2008) Regulation of NKCC2 by a chloride-sensing mechanism involving the WNK3 and SPAK kinases. Proc Natl Acad Sci U S A 105:8458–8463PubMedCrossRefGoogle Scholar
  88. 88.
    Qian Z, Lin C, Espinosa R et al (2001) Cloning and characterization of MST4, a novel Ste20-like kinase. J Biol Chem 276:22439–22445PubMedCrossRefGoogle Scholar
  89. 89.
    Raman M, Earnest S, Zhang K et al (2007) TAO kinases mediate activation of p38 in response to DNA damage. EMBO J 26:2005–2014PubMedCrossRefGoogle Scholar
  90. 90.
    Ramjaun AR, Angers A, Legendre-Guillemin V et al (2001) Endophilin regulates JNK activation through its interaction with the germinal center kinase-like kinase. J Biol Chem 276:28913–28919PubMedCrossRefGoogle Scholar
  91. 91.
    Reszka AA, Halasy-Nagy JM, Masarachia PJ et al (1999) Bisphosphonates act directly on the osteoclast to induce caspase cleavage of mst1 kinase during apoptosis. A link between inhibition of the mevalonate pathway and regulation of an apoptosis-promoting kinase. J Biol Chem 274:34967–34973PubMedCrossRefGoogle Scholar
  92. 92.
    Richardson C, Alessi DR (2008) The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci 121:3293–3304PubMedCrossRefGoogle Scholar
  93. 93.
    Richardson C, Rafiqi FH, Karlsson HK et al (2008) Activation of the thiazide-sensitive Na+-Cl- cotransporter by the WNK-regulated kinases SPAK and OSR1. J Cell Sci 121:675–684PubMedCrossRefGoogle Scholar
  94. 94.
    Sabourin LA, Rudnicki MA (1999) Induction of apoptosis by SLK, a Ste20-related kinase. Oncogene 18:7566–7575PubMedCrossRefGoogle Scholar
  95. 95.
    Sabourin LA, Tamai K, Seale P et al (2000) Caspase 3 cleavage of the Ste20-related kinase SLK releases and activates an apoptosis-inducing kinase domain and an actin-disassembling region. Mol Cell Biol 20:684–696PubMedCrossRefGoogle Scholar
  96. 96.
    Schinkmann K, Blenis J (1997) Cloning and characterization of a human STE20-like protein kinase with unusual cofactor requirements. J Biol Chem 272:28695–28703PubMedCrossRefGoogle Scholar
  97. 97.
    Schneider ME, Dose AC, Salles FT et al (2006) A new compartment at stereocilia tips defined by spatial and temporal patterns of myosin IIIa expression. J Neurosci 26:10243–10252PubMedCrossRefGoogle Scholar
  98. 98.
    Sells MA, Chernoff J (1997) Emerging from the Pak: the p21-activated protein kinase family. Trends Cell Biol 7:162–167PubMedCrossRefGoogle Scholar
  99. 99.
    Shi CS, Kehrl JH (2003) Tumor necrosis factor (TNF)-induced germinal center kinase-related (GCKR) and stress-activated protein kinase (SAPK) activation depends upon the E2/E3 complex Ubc13-Uev1A/TNF receptor-associated factor 2 (TRAF2). J Biol Chem 278:15429–15434PubMedCrossRefGoogle Scholar
  100. 100.
    Shi CS, Huang NN, Harrison K et al (2006) The mitogen-activated protein kinase kinase kinase kinase GCKR positively regulates canonical and noncanonical Wnt signaling in B lymphocytes. Mol Cell Biol 26:6511–6521PubMedCrossRefGoogle Scholar
  101. 101.
    Sonnichsen B, Koski LB, Walsh A et al (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434:462–469PubMedCrossRefGoogle Scholar
  102. 102.
    Stegert MR, Hergovich A, Tamaskovic R et al (2005) Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol Cell Biol 25:11019–11029PubMedCrossRefGoogle Scholar
  103. 103.
    Strange K, Denton J, Nehrke K (2006) Ste20-type kinases: evolutionarily conserved regulators of ion transport and cell volume. Physiology (Bethesda) 21:66–68Google Scholar
  104. 104.
    Su YC, Han J, Xu S et al (1997) NIK is a new Ste20-related kinase that binds NCK and MEKK1 and activates the SAPK/JNK cascade via a conserved regulatory domain. EMBO J 16:1279–1290PubMedCrossRefGoogle Scholar
  105. 105.
    Su YC, Treisman JE, Skolnik EY (1998) The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev 12:2371–2380PubMedCrossRefGoogle Scholar
  106. 106.
    Sung V, Luo W, Qian D et al (2003) The Ste20 kinase MST4 plays a role in prostate cancer progression. Cancer Res 63:3356–3363PubMedGoogle Scholar
  107. 107.
    Taira K, Umikawa M, Takei K et al (2004) The Traf2- and Nck-interacting kinase as a putative effector of Rap2 to regulate actin cytoskeleton. J Biol Chem 279:49488–49496PubMedCrossRefGoogle Scholar
  108. 108.
    Tamari M, Daigo Y, Nakamura Y (1999) Isolation and characterization of a novel serine threonine kinase gene on chromosome 3p22–21.3. J Hum Genet 44:116–120PubMedCrossRefGoogle Scholar
  109. 109.
    Tassi E, Biesova Z, Di Fiore PP et al (1999) Human JIK, a novel member of the STE20 kinase family that inhibits JNK and is negatively regulated by epidermal growth factor. J Biol Chem 274:33287–33295PubMedCrossRefGoogle Scholar
  110. 110.
    Tung RM, Blenis J (1997) A novel human SPS1/STE20 homologue, KHS, activates Jun N-terminal kinase. Oncogene 14:653–659PubMedCrossRefGoogle Scholar
  111. 111.
    Ushiro H, Tsutsumi T, Suzuki K et al (1998) Molecular cloning and characterization of a novel Ste20-related protein kinase enriched in neurons and transporting epithelia. Arch Biochem Biophys 355:233–240PubMedCrossRefGoogle Scholar
  112. 112.
    Villa F, Goebel J, Rafiqi FH et al (2007) Structural insights into the recognition of substrates and activators by the OSR1 kinase. EMBO Rep 8:839–845PubMedCrossRefGoogle Scholar
  113. 113.
    Vitari AC, Deak M, Morrice NA et al (2005) The WNK1 and WNK4 protein kinases that are mutated in Gordon’s hypertension syndrome, phosphorylate and active SPAK and OSR1 protein kinases. Biochem J 391:17–24PubMedCrossRefGoogle Scholar
  114. 114.
    Vitari AC, Thastrup J, Rafiqi FH et al (2006) Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 397:223–231PubMedCrossRefGoogle Scholar
  115. 115.
    Walsh T, Walsh V, Vreugde S et al (2002) From flies’ eyes to our ears: mutations in a human class III myosin cause progressive nonsyndromic hearing loss DFNB30. Proc Natl Acad Sci U S A 99:7518–7523PubMedCrossRefGoogle Scholar
  116. 116.
    Walter SA, Cutler RE Jr, Martinez R et al (2003) Stk10, a new member of the polo-like kinase kinase family highly expressed in hematopoietic tissue. J Biol Chem 278:18221–18228PubMedCrossRefGoogle Scholar
  117. 117.
    Wang Y, O’Connell JR, McArdle PF et al (2009) From the cover: whole-genome association study identifies STK39 as a hypertension susceptibility gene. Proc Natl Acad Sci U S A 106:226–231PubMedCrossRefGoogle Scholar
  118. 118.
    Willatt L, Cox J, Barber J et al (2005) 3q29 microdeletion syndrome: clinical and molecular characterization of a new syndrome. Am J Hum Genet 77:154–160PubMedCrossRefGoogle Scholar
  119. 119.
    Wu MF, Wang SG (2008) Human TAO kinase 1 induces apoptosis in SH-SY5Y cells. Cell Biol Int 32:151–156PubMedCrossRefGoogle Scholar
  120. 120.
    Wu S, Huang J, Dong J et al (2003) Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114:445–456PubMedCrossRefGoogle Scholar
  121. 121.
    Xue Y, Wang X, Li Z et al (2001) Mesodermal patterning defect in mice lacking the Ste20 NCK interacting kinase (NIK). Development 128:1559–1572PubMedGoogle Scholar
  122. 122.
    Yang F, Li X, Sharma M et al (2001) Androgen receptor specifically interacts with a novel p21-activated kinase, PAK6. J Biol Chem 276:15345–15353PubMedCrossRefGoogle Scholar
  123. 123.
    Yustein JT, Xia L, Kahlenburg JM et al (2003) Comparative studies of a new subfamily of human Ste20-like kinases: homodimerization, subcellular localization, and selective activation of MKK3 and p38. Oncogene 22:6129–6141PubMedCrossRefGoogle Scholar
  124. 124.
    Zenke FT, King CC, Bohl BP et al (1999) Identification of a central phosphorylation site in p21-activated kinase regulating autoinhibition and kinase activity. J Biol Chem 274:32565–32573PubMedCrossRefGoogle Scholar
  125. 125.
    Zhao ZS, Manser E, Chen XQ et al (1998) A conserved negative regulatory region in alphaPAK: inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1. Mol Cell Biol 18:2153–2163PubMedGoogle Scholar
  126. 126.
    Zhou T, Raman M, Gao Y et al (2004) Crystal structure of the TAO2 kinase domain: activation and specificity of a Ste20p MAP3K. Structure 12:1891–1900PubMedCrossRefGoogle Scholar
  127. 127.
    Zhu G, Fujii K, Liu Y et al (2005) A single pair of acidic residues in the kinase major groove mediates strong substrate preference for P-2 or P-5 arginine in the AGC, CAMK, and STE kinase families. J Biol Chem 280:36372–36379PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of AnesthesiologyVanderbilt University Medical CenterNashvilleUSA

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