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Tyrosine kinase Hck

Sarah Cook '11 and Sally Moseley '12


Contents:


I. Introduction

Tyrosine phosphorylation has roles in cell proliferation, migration, differentiation, and survival (Thomas et al. 1997). A family of kinases that participate in tyrosine phosphorylation is the Src kinase family.  Members of this kinase family phosphorylate a variety of substrates involved in many cellular processes.  The Src kinases’ ability to act on many different substrates allows for the diversity of effects that result from their phosphorylase activity. 

This Src kinase family was first discovered with the finding that a member of this familiy, v-src, is implicated in Rous sarcoma virus.  This viral form of src leads to rapid tyrosine phosphorylation in the cytoplasm of host cells, making it a powerful cellular transforming agent.  Therefore, a greater understanding of these kinases is important for understanding the signal transduction pathways involved in human viruses. 

All Src kinase family enzymes are composed of 3 conserved domains and kinase-specific linker between 2 of the three domains.  This linker allows for interactions specific to each kinase’s function. Here, a member of this family, tyrosine kinase Hck, is reviewed.  Hck was crystallized as a dimer .  Hck is found in lymphoid and myeloid cells bound to B-cell receptors in inactive B cells.  A lack of Hck results in developmental defects and suppressed immunity. 

 



II. General Structure

The tyrosine kinase Hck is composed of four parts: the catalytic domain, the SH2 domain, the SH3 domain, and the linker .  The catalytic domain is composed of a N-lobe and a C-lobe , which interact with phosphate groups and other substrates, respectively, and is responsible for tyrosine kinase activity.  The N-lobe is composed of mostly β sheets, allowing for its interactions with incoming phosphate groups .  The C-lobe is composed of mostly α-helicies, which bind substrates in the substrate binding groove .   The SH2 and SH3 domains are bound to the catalytic domain on the side opposite its active site and provide stability and regulation of the catalytic domain .  The SH2 domain is made up of 3 major β sheets and 2 α helicies .  SH2 is bound to the C- lobe of the catalytic domain via a phosphotyrosine residue (residue 527) and Pro 531 on the C-lobe .  Because there are three residues between the phosphotyrosine residue and Pro 531, the peptide bends away from the SH2 domain (link), creating a lower-affinity interaction SH2 is also connected to the N-lobe of the catalytic domain by a polyproline type II (PPII) helix that spans from residues Pro 244 to Trp 254 .  The hydrophobic surface of the third domain SH3 is created by 5 β sheets , which allows it to bind to the SH2-kinase linker.  The hydrophobic surface of the third domain SH3 binds to this SH2-kinase linker .  This linker gives Hck much of its protein specificity because the sequence of the linker is highly variable amongst Src kinases. 


III. Phosphorylation

Kinase activity is correlated to the conformation of the protein. The 'closed' conformation is the active form because the two lobes of the catalytic site bring the phosphate group and substrate into closer proximity. The 'open' conformation is the inactive form because the lobes are bent away from each other, disallowing interactions between the phosphate group and substrate. 

Hck's conformation as either 'closed' or 'open' is dependent on autophosphorylation at Tyr 416. When unphosphorylated, Glu 310 on an α-helix, αC, of the N-lobe of the catalytic domain forms a hydrogen bond with Arg 385 , causing Glu 310 to be flipped outward. In this inactive state, SH3 is bound to the SH2-kinase linker via residue Trp 260 on SH3 and αC on the N-lobe of the catalytic domain . Alternately, when Tyr 416 in the activation segment of the catalytic domain is phosphorylated, the phosphorylated tyrosine interacts with Arg 385 , barring the Glu 310-Arg 385 interaction. In this conformation, Glu 310 and αC are able to rotate inward, causing the release of SH3 from the SH2-kinase linker. The flexible linker allows the enzyme to adopt the active conformation.


IV. Comparison to PKA

The structure of tyrosine kinase Hck has many similarities to that of cyclic-AMP-dependent protein kinase A (PKA) complexed with ATP .  The active sites of Hck and ATP-bound PKA have very similar conformations and superimposition of the two kinases shows only a 3° difference in the angles between the N- and C-lobes (link). This similarity to active ATP-bound PKA is important because it shows that Hck is also in its active conformation.  The N- lobe is slightly further from the C- lobe in Hck, overlapping the normal position αC in PKA.  Due to this slight difference in configuration, some residues on αC in each enzyme are facing different directions (link)In PKA, the Glu 91 residue, equivalent to Glu 310 in Hck, faces inward forming an ionic bond with Lys 72 , which directs the α- and β-phosphates of ATP.  The charged Glu 91 adjacent to Lys 72 plays a large role in PKA’s enzymatic activity.  Hck deals with having an outward facing Glu 310 by the phosphorylation-dependent conformation change described in the above section .  This allows for a unique allosteric regulation of Hck.



V. Applications

Over-activation of Hck may lead to stunted cell growth, as evidenced by its association with unstimulated B-cells (Sicheri et al., 1997) and suppressed growth of mutated yeast cells with Src expression (Trible et al., 2006).  This could be part of the mechanism by which oncoviruses disrupt cell activity.  Nef, an HIV-1 protein, increases viral pathogenicity by activating Src family kinases that initialize a signal transduction pathway (Trible et al., 2006).

Therefore, Hck is also claimed to be an essential factor in the progression of the disease to acquired immune deficiency syndrome (AIDS) (Choi et al., 2004).  In the absence of Nef, autophosphorylation of Tyr 416 is a slow process involving the subunits SH2 and SH3 and ATP.  The two subunits SH3 and the catalytic domain continue to associate with each other.  In the presence of Nef, however, SH3 binds to Nef and is completely detached from the catalytic domain and only associated with the SH2.  This leaves Hck in an extended, open conformation that allows rapid phosphorylation of Tyr 416 and thus maximizes the activation of the kinase.  It is possible that Hck’s enhanced activity in the presence of Nef in HIV-infected people may have something to do with Hck’s correlation with unstimulated B cells.  If hightened Hck activity causes the inactivity of B cells, the suppression of the immune system that comes with HIV could be due to inactive B cells.


VI. References

Choi, Hyun-Jung and Thomas E. Smithgall.  2004  Conserved Residues in the HIV-1 Nef Hydrophobic Pocket are Essential for Recruitment and Activation of the Hck Tyrosine Kinase.  Journal of Molecular Biology 5:1255-1268

Sicheri, Frank, Ismail Moarefi, and John Kuriyan.  1997. Crystal structure of the Src family tyrosine kinase Hck. Nature 385: 602-609.

Thomas, S. M. and J. S. Brugge. 1997. Cellular Functions Regulated by SRC Family Kinases. Annu. Rev. Cell Dev. Biol. 13: 513-609.

Trible, Ronald P., Lory Emert-Sedlak, and Thomas E. Smithgall. 2006.  HIV-1 Nef selectively activates Src family kinases Hck, Lyn, and c-Src through direct SH3 domain interaction. Journal of Biological Chemistry 281: 27029-38.

Zheng, Jianhua, Elzbieta A. Trafny, Daniel R. Knighton, Nguyen-Huu Xuong, Susan S. Taylor, Lynn F. Ten Eyck, and Janusz M. Sowadski.  1992. A refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Cryst. 49: 362-365.

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