PHLPP2 is a pseudophosphatase that lost activity in the metazoan ancestor

T Tarik Husremović (Max Perutz Labs, University of Vienna and Medical University of Vienna) V Vanessa Meier (Max Perutz Labs, University of Vienna and Medical University of Vienna) L Lucas Piëch (Max Perutz Labs, University of Vienna and Medical University of Vienna) K Katharina M. Siess (Max Perutz Labs, University of Vienna and Medical University of Vienna) S Sumire Antonioli (Max Perutz Labs, University of Vienna and Medical University of Vienna) I Irina Grishkovskaya (Research Institute of Molecular Pathology, Vienna BioCenter) N Nikoleta Kircheva (Institute of Optical Materials and Technologies “Acad. J. Malinowski”, Bulgarian Academy of Sciences) S Silvia E. Angelova (Institute of Optical Materials and Technologies “Acad. J. Malinowski”, Bulgarian Academy of Sciences) K Karoline Wenzl (Max Perutz Labs, University of Vienna and Medical University of Vienna) A Andreas Brandstätter (Department of Chemistry, Institute of Analytical Chemistry, University of Natural Resources and Life Sciences) J Jiri Veis (Max Perutz Labs, University of Vienna and Medical University of Vienna) F Fran Miočić-Stošić (Max Perutz Labs, University of Vienna and Medical University of Vienna) D Dorothea Anrather (Max Perutz Labs, Mass Spectrometry Facility, Vienna Biocenter Campus) M Markus Hartl (Max Perutz Labs, Mass Spectrometry Facility, Vienna Biocenter Campus) L Linda Truebestein (Max Perutz Labs, University of Vienna and Medical University of Vienna) L Luis M. Cerron-Alvan (Max Perutz Labs, University of Vienna and Medical University of Vienna) M Martin Leeb (Max Perutz Labs, University of Vienna and Medical University of Vienna) B Bojan Žagrović (Max Perutz Labs, University of Vienna and Medical University of Vienna) S Stephan Hann (Department of Chemistry, Institute of Analytical Chemistry, University of Natural Resources and Life Sciences) C Christoph Bock E Egon Ogris (Max Perutz Labs, University of Vienna and Medical University of Vienna) T Todor Dudev (Faculty of Chemistry and Pharmacy, Sofia University “St. Kliment Ohridski”) N Nicholas A. T. Irwin (Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter) D David Haselbach (Research Institute of Molecular Pathology, Vienna BioCenter) T Thomas A. Leonard (Max Perutz Labs, University of Vienna and Medical University of Vienna)

Abstract

The phosphoinositide 3-kinase (PI3K) pathway is a major regulator of cell and organismal growth. Consequently, hyperactivation of PI3K and its downstream effector kinase, Akt, is observed in many human cancers. Pleckstrin homology domain leucine-rich repeat-containing protein phosphatases (PHLPP), two paralogous members of the metal-dependent protein phosphatase family, have been reported as negative regulators of Akt signaling and, therefore, tumor suppressors. However, the stoichiometry and identity of the bound metal ion(s), mechanism of action, and enzymatic specificity of these proteins are not known. Seeking to fill these gaps in our understanding of PHLPP biology, we unexpectedly found that PHLPP2 has no catalytic activity in vitro. Instead, we found that PHLPP2 is a pseudophosphatase with a single zinc ion bound in its catalytic center. Furthermore, we found that cancer genomics data do not support the proposed role of PHLPP1 or PHLPP2 as tumor suppressors. Phylogenetic analyses revealed an ancestral phosphatase that arose more than 1,000 Mya, but that lost activity at the base of the metazoan lineage. Surface conservation indicates that while PHLPP2 has lost catalytic activity, it may have retained substrate binding. Finally, using phylogenomics, we identify coevolving genes consistent with a scaffolding role for PHLPP2 on membranes. In summary, our results provide a molecular explanation for the inconclusive results that have hampered research on PHLPP and argue for a focus on the noncatalytic roles of PHLPP1 and PHLPP2.

Article Details

Volume / Issue Vol. 122, Issue 14
Published April 08, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (25)

T

Tarik Husremović

Max Perutz Labs, University of Vienna and Medical University of Vienna

V

Vanessa Meier

Max Perutz Labs, University of Vienna and Medical University of Vienna

L

Lucas Piëch

Max Perutz Labs, University of Vienna and Medical University of Vienna

K

Katharina M. Siess

Max Perutz Labs, University of Vienna and Medical University of Vienna

S

Sumire Antonioli

Max Perutz Labs, University of Vienna and Medical University of Vienna

I

Irina Grishkovskaya

Research Institute of Molecular Pathology, Vienna BioCenter

N

Nikoleta Kircheva

Institute of Optical Materials and Technologies “Acad. J. Malinowski”, Bulgarian Academy of Sciences

S

Silvia E. Angelova

Institute of Optical Materials and Technologies “Acad. J. Malinowski”, Bulgarian Academy of Sciences

K

Karoline Wenzl

Max Perutz Labs, University of Vienna and Medical University of Vienna

A

Andreas Brandstätter

Department of Chemistry, Institute of Analytical Chemistry, University of Natural Resources and Life Sciences

J

Jiri Veis

Max Perutz Labs, University of Vienna and Medical University of Vienna

F

Fran Miočić-Stošić

Max Perutz Labs, University of Vienna and Medical University of Vienna

D

Dorothea Anrather

Max Perutz Labs, Mass Spectrometry Facility, Vienna Biocenter Campus

M

Markus Hartl

Max Perutz Labs, Mass Spectrometry Facility, Vienna Biocenter Campus

L

Linda Truebestein

Max Perutz Labs, University of Vienna and Medical University of Vienna

L

Luis M. Cerron-Alvan

Max Perutz Labs, University of Vienna and Medical University of Vienna

M

Martin Leeb

Max Perutz Labs, University of Vienna and Medical University of Vienna

B

Bojan Žagrović

Max Perutz Labs, University of Vienna and Medical University of Vienna

S

Stephan Hann

Department of Chemistry, Institute of Analytical Chemistry, University of Natural Resources and Life Sciences

C

Christoph Bock

E

Egon Ogris

Max Perutz Labs, University of Vienna and Medical University of Vienna

T

Todor Dudev

Faculty of Chemistry and Pharmacy, Sofia University “St. Kliment Ohridski”

N

Nicholas A. T. Irwin

Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter

D

David Haselbach

Research Institute of Molecular Pathology, Vienna BioCenter

T

Thomas A. Leonard

Max Perutz Labs, University of Vienna and Medical University of Vienna