Pyrvinium attenuates Hedgehog signaling downstream of smoothened.

The Hedgehog (HH) signaling pathway represents an important class of emerging developmental signaling pathways that play critical roles in the genesis of a large number of human cancers. The pharmaceutical industry is currently focused on developing small molecules targeting Smoothened (Smo), a key signaling effector of the HH pathway that regulates the levels and activity of the Gli family of transcription factors. Although one of these compounds, vismodegib, is now FDA-approved for patients with advanced basal cell carcinoma, acquired mutations in Smo can result in rapid relapse. Furthermore, many cancers also exhibit a Smo-independent activation of Gli proteins, an observation that may underlie the limited efficacy of Smo inhibitors in clinical trials against other types of cancer. Thus, there remains a critical need for HH inhibitors with different mechanisms of action, particularly those that act downstream of Smo. Recently, we identified the FDA-approved anti-pinworm compound pyrvinium as a novel, potent (IC50, 10 nmol/L) casein kinase-1α (CK1α) agonist. We show here that pyrvinium is a potent inhibitor of HH signaling, which acts by reducing the stability of the Gli family of transcription factors. Consistent with CK1α agonists acting on these most distal components of the HH signaling pathway, pyrvinium is able to inhibit the activity of a clinically relevant, vismodegib -resistant Smo mutant, as well as the Gli activity resulting from loss of the negative regulator suppressor of fused. We go on to demonstrate the utility of this small molecule in vivo, against the HH-dependent cancer medulloblastoma, attenuating its growth and reducing the expression of HH biomarkers.

[1]  C. Girardi,et al.  Pyrvinium pamoate does not activate protein kinase CK1, but promotes Akt/PKB down-regulation and GSK3 activation. , 2013, The Biochemical journal.

[2]  M. Salgaller American Association for Cancer Research , 2000, Expert opinion on investigational drugs.

[3]  James M. Olson,et al.  Medulloblastoma Growth Inhibition by Hedgehog Pathway Blockade , 2002, Science.

[4]  S. Thiyagarajan,et al.  Gli2 Is Targeted for Ubiquitination and Degradation by β-TrCP Ubiquitin Ligase* , 2006, Journal of Biological Chemistry.

[5]  T. Januario,et al.  Pharmacokinetic–Pharmacodynamic Analysis of Vismodegib in Preclinical Models of Mutational and Ligand-Dependent Hedgehog Pathway Activation , 2011, Clinical Cancer Research.

[6]  Lawrence Lum,et al.  Identification of Hedgehog Pathway Components by RNAi in Drosophila Cultured Cells , 2003, Science.

[7]  D. Mathews,et al.  Pyrvinium pamoate changes alternative splicing of the serotonin receptor 2C by influencing its RNA structure , 2013, Nucleic acids research.

[8]  M. Lauth,et al.  Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. , 2006, Developmental cell.

[9]  Zainab Jagani,et al.  Unraveling the therapeutic potential of the Hedgehog pathway in cancer , 2013, Nature Medicine.

[10]  A. Joyner,et al.  Sonic hedgehog Signaling Regulates Gli2 Transcriptional Activity by Suppressing Its Processing and Degradation , 2006, Molecular and Cellular Biology.

[11]  S. Thiyagarajan,et al.  Gli2 is targeted for ubiquitination and degradation by beta-TrCP ubiquitin ligase. , 2006, The Journal of biological chemistry.

[12]  M. Scott,et al.  Communicating with Hedgehogs , 2005, Nature Reviews Molecular Cell Biology.

[13]  J. Concordet,et al.  Multisite Protein Kinase A and Glycogen Synthase Kinase 3β Phosphorylation Leads to Gli3 Ubiquitination by SCFβTrCP , 2006, Molecular and Cellular Biology.

[14]  C. Hui,et al.  Cilium – independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved , 2009 .

[15]  R. Ahrends,et al.  Gli protein activity is controlled by multisite phosphorylation in vertebrate Hedgehog signaling. , 2014, Cell reports.

[16]  S. Kaesler,et al.  Suppression of casein kinase 1alpha in melanoma cells induces a switch in beta-catenin signaling to promote metastasis. , 2010, Cancer research.

[17]  R. Lipinski,et al.  Establishment and characterization of immortalized Gli-null mouse embryonic fibroblast cell lines , 2008, BMC Cell Biology.

[18]  Yanyun Li,et al.  Evidence for the direct involvement of βTrCP in Gli3 protein processing , 2006 .

[19]  Ethan Lee,et al.  LRP6 transduces a canonical Wnt signal independently of Axin degradation by inhibiting GSK3's phosphorylation of β-catenin , 2008, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Concordet,et al.  Multisite protein kinase A and glycogen synthase kinase 3beta phosphorylation leads to Gli3 ubiquitination by SCFbetaTrCP. , 2006, Molecular and cellular biology.

[21]  C. Rudin,et al.  Smoothened Mutation Confers Resistance to a Hedgehog Pathway Inhibitor in Medulloblastoma , 2009, Science.

[22]  M. Scott,et al.  Control of Neuronal Precursor Proliferation in the Cerebellum by Sonic Hedgehog , 1999, Neuron.

[23]  D. Robbins,et al.  The Hedgehog Signal Transduction Network , 2012, Science Signaling.

[24]  Y. Harada,et al.  Pyrvinium pamoate inhibits proliferation of myeloma/erythroleukemia cells by suppressing mitochondrial respiratory complex I and STAT3. , 2012, Cancer letters.

[25]  Steffen Jung,et al.  CKIα ablation highlights a critical role for p53 in invasiveness control , 2011, Nature.

[26]  M. Scott,et al.  The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. , 2010, Genes & development.

[27]  H. Esumi,et al.  An anticancer agent, pyrvinium pamoate inhibits the NADH-fumarate reductase system--a unique mitochondrial energy metabolism in tumour microenvironments. , 2012, Journal of biochemistry.

[28]  M. Karagas,et al.  Activation of Hedgehog signaling by the environmental toxicant arsenic may contribute to the etiology of arsenic-induced tumors. , 2010, Cancer research.

[29]  Bruce J. Melancon,et al.  Small-molecule inhibition of Wnt signaling through activation of casein kinase 1α. , 2010, Nature chemical biology.

[30]  J. Briscoe,et al.  Sonic Hedgehog Dependent Phosphorylation by CK1α and GRK2 Is Required for Ciliary Accumulation and Activation of Smoothened , 2011, PLoS biology.

[31]  Chengbing Wang,et al.  Phosphorylation of Gli2 by protein kinase A is required for Gli2 processing and degradation and the Sonic Hedgehog-regulated mouse development. , 2009, Developmental biology.

[32]  M. Stöter,et al.  IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and -epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects , 2000, Oncogene.

[33]  Yanyun Li,et al.  Evidence for the direct involvement of {beta}TrCP in Gli3 protein processing. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Angers,et al.  Gli proteins in development and disease. , 2011, Annual review of cell and developmental biology.

[35]  M. Scott,et al.  Altered neural cell fates and medulloblastoma in mouse patched mutants. , 1997, Science.

[36]  Marie Evangelista,et al.  Kinetics of Hedgehog-Dependent Full-Length Gli3 Accumulation in Primary Cilia and Subsequent Degradation , 2010, Molecular and Cellular Biology.

[37]  H. Weiner,et al.  The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. , 2001, Development.

[38]  C. Cruciat,et al.  RNA Helicase DDX3 Is a Regulatory Subunit of Casein Kinase 1 in Wnt–β-Catenin Signaling , 2013, Science.

[39]  C. McClung,et al.  An inhibitor of casein kinase 1 &egr;/&dgr; partially normalizes the manic-like behaviors of the Clock&Dgr;19 mouse , 2012, Behavioural pharmacology.

[40]  B. Wang,et al.  Multiple Ser/Thr-rich degrons mediate the degradation of Ci/Gli by the Cul3-HIB/SPOP E3 ubiquitin ligase , 2009, Proceedings of the National Academy of Sciences.

[41]  R. Toftgård,et al.  Hedgehog beyond medulloblastoma and basal cell carcinoma. , 2010, Biochimica et biophysica acta.

[42]  Allon M Klein,et al.  Kinetic Responses of β-Catenin Specify the Sites of Wnt Control , 2012, Science.

[43]  W. Schulz-Schaeffer,et al.  Time-point and dosage of gene inactivation determine the tumor spectrum in conditional Ptch knockouts. , 2009, Carcinogenesis.

[44]  D. Virshup,et al.  Casein kinase 1: Complexity in the family. , 2011, The international journal of biochemistry & cell biology.

[45]  Timothy H. Davis,et al.  Pyrvinium Targets the Unfolded Protein Response to Hypoglycemia and Its Anti-Tumor Activity Is Enhanced by Combination Therapy , 2008, PloS one.

[46]  Philip A Beachy,et al.  Hedgehog-Regulated Processing of Gli3 Produces an Anterior/Posterior Repressor Gradient in the Developing Vertebrate Limb , 2000, Cell.

[47]  Jun Zhang,et al.  Casein kinase 1α governs antigen-receptor-induced NF-κB activation and human lymphoma cell survival , 2009, Nature.

[48]  K. Bussell,et al.  Systems biology: The dynamics of the cycle , 2005, Nature Reviews Molecular Cell Biology.

[49]  M. Scott,et al.  Patched 1 Regulates Hedgehog Signaling at the Primary Cilium , 2022 .

[50]  A. Salic,et al.  A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu–Gli protein complexes , 2010, The Journal of cell biology.

[51]  S. Qin,et al.  Casein Kinase 1α Interacts with Retinoid X Receptor and Interferes with Agonist-induced Apoptosis* , 2004, Journal of Biological Chemistry.