*179050
PYRUVATE KINASE, MUSCLE, 2; PKM2

Alternative titles; symbols
PYRUVATE KINASE 3; PK3
PKM
OPA-INTERACTING PROTEIN 3; OIP3
THYROID HORMONE-BINDING PROTEIN, CYTOSOLIC; THBP1

Other entities represented in this entry:
PYRUVATE KINASE, MUSCLE, 1, INCLUDED; PKM1, INCLUDED

HGNC Approved Gene Symbol: PKM2

Cytogenetic location: 15q23     Genomic coordinates (GRCh37): 15:72,491,369 - 72,523,726 (from NCBI)

TEXT
Description
Pyruvate kinase (ATP:pyruvate phosphotransferase, EC 2.7.1.40) is a glycolytic enzyme that catalyzes the transfer of a phosphoryl group from phosphoenolpyruvate (PEP) to ADP, generating ATP (Ikeda and Noguchi, 1998).

Cloning
Tsutsumi et al. (1988) showed that pyruvate kinase occurs in 4 isozymic forms (L, R, M1, M2) and that these are encoded by 2 different genes, PKLR (609712) and PKM2. The L and R isozymes are generated from the PKLR gene by differential splicing of RNA; the M1 and M2 forms are produced from the PKM2 gene by differential splicing. Northern blot analysis with RNA from a human hepatoma demonstrated that the M2-type PK was predominantly expressed in hepatoma cells, whereas L-type PK was preferentially expressed in the nontumor portion of the liver.

Kitagawa et al. (1987) purified a human cytosolic thyroid hormone-binding protein (THBP1; p58) from human epidermoid carcinoma cells, which comprised a single polypeptide chain with a molecular mass of 58 kD. The sequence of the cDNA for p58 indicated that it was homologous to pyruvate kinase subtype M2.

Gene Structure
Takenaka et al. (1991) reported that the gene that encodes both the M1 and the M2 isozymes is approximately 32 kb long and comprises 12 exons and 11 introns. Exons 9 and 10 contain sequences specific for the M1 and M2 types, respectively, indicating that the human fetal and adult isozymes are produced from the same gene by alternative splicing. The gene is transcribed from multiple start sites, and the 5-prime flanking region contains putative SP1 (189906)-binding sites, but no TATA or CAAT boxes.

Gene Function
The activity of pyruvate kinase subtype M2 is increased by fructose 1,6-bisphosphate (Fru-1,6-P2). Ashizawa et al. (1991) manipulated the intracellular Fru-1,6-P2 concentration in several mammalian cell lines, including human, by varying the glucose concentration in the media. Glucose rapidly and reversibly changed the ratio of cytosolic monomeric PKM2 to tetrameric PKM2. In the physiologic range of glucose, the majority of PKM2 existed as tetramer. However, tetrameric PKM2 dissociated into monomeric form within minutes after cells were deprived of glucose, thus shutting off the glycolytic pathway. Inhibition of glucose uptake through its specific transporter also converted the tetramer to the monomeric form within 20 to 30 minutes. Ashizawa et al. (1991) concluded that Fru-1,6-P2 is the metabolite in the glycolytic pathway that regulates PK activity.

The M1 and M2 isozymes of PK differ by 21 amino acids, and the region in which they differ encodes the 2 alpha helices that participate in intersubunit contact. While the M2 isozyme is activated homotropically by phosphoenolpyruvate and heterotropically by Fru-1,6-P2, the M1 isozyme remains fully active, likely due to its intrinsic active conformation. Ikeda and Noguchi (1998) determined that cys423, located in the vicinity of the second alpha helix in rat Pkm2, plays an important role in the allosteric effect of the M2 isozyme.

Neisseria gonorrhoeae opacity-associated (Opa) proteins are a family of outer membrane proteins involved in gonococcal adhesion to and invasion of human cells. Opa expression appears to be necessary for gonococcal disease. Using the yeast 2-hybrid system to screen a HeLa cell cDNA library with an N. gonorrhoeae Opa protein as bait, Williams et al. (1998) identified partial cDNAs encoding Opa-interacting protein-1 (OIP1, or TRIP6; 602933), OIP2 (606019), OIP3, OIP4 (PRAME; 606021), and OIP5 (606020). Sequence analysis predicted that the partial OIP3 cDNA encodes a 164-amino acid peptide that is 100% identical to the C-terminal third of PKM2. OIP3 contains a cluster of basic residues, but unlike OIP1, OIP4, and OIP5, it has no cysteine motif. Binding analysis confirmed the interaction of OIP3 with Opa. Gonococcal strains not expressing Opa bound OIP3, or PK, weakly compared with Opa-positive strains. Immunofluorescence microscopy demonstrated that intracellular but not extracellular Opa-positive gonococci colocalized with PK in endocervical epithelial cells. Opa-negative bacteria did not colocalize with PK. Mutation analysis indicated that pyruvate is required as a substrate for the intracellular survival and growth of N. gonorrhoeae. Williams et al. (1998) proposed that gonococci acquire host PK on their surface to create a microenvironment rich in pyruvate for growth.

Using a novel proteomic screen for phosphotyrosine-binding proteins, Christofk et al. (2008) observed that PKM2 binds directly and selectively to tyrosine-phosphorylated peptides. The authors showed that binding of phosphotyrosine peptides to PKM2 results in release of the allosteric activator fructose-1,6-bisphosphate, leading to inhibition of PKM2 enzymatic activity. Christofk et al. (2008) also provided evidence that this regulation of PKM2 by phosphotyrosine signaling diverts glucose metabolites from energy production to anabolic processes when cells are stimulated by certain growth factors. Collectively, Christofk et al. (2008) concluded that expression of this phosphotyrosine-binding form of pyruvate kinase is critical for rapid growth in cancer cells.

Christofk et al. (2008) showed that a single switch in a splice isoform of the glycolytic enzyme pyruvate kinase is necessary for the shift in cellular metabolism to aerobic glycolysis and that this shift promotes tumorigenesis. Tumor cells express exclusively the embryonic M2 isoform of pyruvate kinase. Christofk et al. (2008) used short hairpin RNA to knock down pyruvate kinase M2 expression in human cancer cell lines and replace it with pyruvate kinase M1. Switching pyruvate kinase expression to the M1 (adult) isoform led to reversal of the Warburg effect, which is the persistence of high lactate production by tumors in the presence of oxygen, as judged by reduced lactate production and increased oxygen consumption, and this correlated with a reduced ability to form tumors in nude mouse xenografts. Christofk et al. (2008) concluded that M2 expression is necessary for aerobic glycolysis and that this metabolic phenotype provides a selective growth advantage for tumor cells in vivo.

The embryonic pyruvate kinase isoform PKM2 is almost universally reexpressed in cancer and promotes aerobic glycolysis, whereas the adult isoform PKM1 promotes oxidative phosphorylation (summarized by David et al., 2010). These 2 isoforms result from mutually exclusive alternative splicing of the PKM pre-mRNA, reflecting inclusion of exon 9 (PKM1) or exon 10 (PKM2). David et al. (2010) showed that 3 heterogeneous nuclear ribonucleoprotein (hnRNP) proteins, polypyrimidine tract-binding protein (PTB, also known as hnRNPI; 600693), hnRNPA1 (164017), and hnRNPA2 (600124), bind repressively to sequences flanking exon 9 of the PKM2 gene, resulting in exon 10 inclusion and the expression of the PKM2 isoform. David et al. (2010) also demonstrated that the oncogenic transcription factor c-MYC (190080) upregulates transcription of PTB, hnRNPA1, and hnRNPA2, ensuring a high PKM2/PKM1 ratio. Establishing a relevance to cancer, David et al. (2010) showed that human gliomas (137800) overexpress c-Myc, PTB, hnRNPA1, and hnRNPA2 in a manner that correlates with PKM2 expression. David et al. (2010) concluded that their results defined a pathway that regulates an alternative splicing event required for tumor cell proliferation.

Anastasiou et al. (2011) showed that, in human lung cancer cells, acute increases in intracellular concentrations of reactive oxygen species caused inhibition of the glycolytic enzyme PKM2 through oxidation of cysteine at position 358. This inhibition of PKM2 is required to divert glucose flux into the pentose phosphate pathway and thereby generate sufficient reducing potential for detoxification of reactive oxygen species. Lung cancer cells in which endogenous PKM2 was replaced with the cys358-to-ser oxidation-resistant mutant exhibited increased sensitivity to oxidative stress and impaired tumor formation in a xenograft model. Anastasiou et al. (2011) concluded that besides promoting metabolic changes required for proliferation, the regulatory properties of PKM2 may confer an additional advantage to cancer cells by allowing them to withstand oxidative stress.

Yang et al. (2011) demonstrated in human cancer cells that EGFR (131550) activation induces translocation of PKM2, but not PKM1, into the nucleus, where K433 of PKM2 binds to c-Src-phosphorylated Y333 of beta-catenin (116806). This interaction is required for both proteins to be recruited to the CCND1 (168461) promoter, leading to HDAC3 (605166) removal from the promoter, histone H3 acetylation, and cyclin D1 expression. PKM2-dependent beta-catenin transactivation is instrumental in EGFR-promoted tumor cell proliferation and brain tumor development. In addition, positive correlations were identified between c-Src activity, beta-catenin Y333 phosphorylation, and PKM2 nuclear accumulation in human glioblastoma specimens. Furthermore, levels of beta-catenin phosphorylation and nuclear PKM2 were correlated with grades of glioma malignancy and prognosis. Yang et al. (2011) concluded that their findings revealed that EGF induces beta-catenin transactivation via a mechanism distinct from that induced by Wnt/Wingless (see 164820) and highlighted the essential nonmetabolic functions of PKM2 in EGFR-promoted beta-catenin transactivation, cell proliferation, and tumorigenesis.

Biochemical Features
The M2 isoform of pyruvate kinase (PKM2) promotes the metabolism of glucose by aerobic glycolysis and contributes to anabolic metabolism. Paradoxically, decreased pyruvate kinase enzyme activity accompanies the expression of PKM2 in rapidly dividing cancer cells and tissues. Vander Heiden et al. (2010) demonstrated that phosphoenolpyruvate (PEP), the substrate for pyruvate kinase in cells, can act as a phosphate donor in mammalian cells because PEP participates in the phosphorylation of the glycolytic enzyme phosphoglycerate mutase (PGAM1; 172250) in PKM2-expressing cells. Vander Heiden et al. (2010) used mass spectrometry to show that the phosphate from PEP is transferred to the catalytic histidine (His11) on human PGAM1. This reaction occurred at physiologic concentrations of PEP and produced pyruvate in the absence of PKM2 activity. The presence of histidine-phosphorylated PGAM2 correlated with the expression of PKM2 in cancer cell lines and tumor tissues. Thus, Vander Heiden et al. (2010) concluded that decreased pyruvate kinase activity in PKM2-expressing cells allows PEP-dependent histidine phosphorylation of PGAM1 and may provide an alternate glycolytic pathway that decouples adenosine triphosphate production from PEP-mediated phosphotransfer, allowing for the high rate of glycolysis to support the anabolic metabolism observed in many proliferating cells.

Mapping
Tani et al. (1988) isolated and sequenced 2 overlapping clones covering the entire coding sequence of PKM2. By in situ hybridization, they demonstrated that the PKM2 gene is located at band 15q22. By in situ hybridization, Popescu and Cheng (1990) mapped the THBP1 gene to 15q24-q25.

Studies of somatic cell hybrids showed that the PK3 and MPI loci are syntenic (Shows, 1972). By cell hybridization studies, Van Heyningen et al. (1975) found that the MPI (154550) and PK3 loci are on chromosome 15. Chern et al. (1977) narrowed the assignment to 15q22-qter.

Molecular Genetics
Data on gene frequencies of allelic variants were tabulated by Roychoudhury and Nei (1988).

See Also:
Chern and Croce (1975); Junien et al. (1980); Kahn et al. (1978); Levine et al. (1978); Ritter et al. (1974); Shows (1973); Westerveld et al. (1975)

REFERENCES
1. Anastasiou, D., Poulogiannis, G., Asara, J. M., Boxer, M. B., Jiang, J., Shen, M., Bellinger, G., Sasaki, A. T., Locasale, J. W., Auld, D. S., Thomas, C. J., Vander Heiden, M. G., Cantley, L. C. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334: 1278-1283, 2011. [PubMed: 22052977, related citations] [Full Text: HighWire Press, Pubget]

2. Ashizawa, K., Willingham, M. C., Liang, C.-M., Cheng, S. In vivo regulation of monomer-tetramer conversion of pyruvate kinase subtype M-2 by glucose is mediated via fructose 1,6-bisphosphate. J. Biol. Chem. 266: 16842-16846, 1991. [PubMed: 1885610, related citations] [Full Text: HighWire Press, Pubget]

3. Chern, C. J., Croce, C. M. Confirmation of the synteny of the human genes for mannose phosphate isomerase and pyruvate kinase and of their assignment to chromosome 15. Cytogenet. Cell Genet. 15: 299-305, 1975. [PubMed: 1222586, related citations] [Full Text: Pubget]

4. Chern, C. J., Kennett, R., Engel, L. E., Mellman, W. J., Croce, C. M. Assignment of the structural genes for the alpha subunit of hexosaminidase A, mannosephosphate isomerase and pyruvate kinase to the region q22-qter of human chromosome 15. Somat. Cell Genet. 3: 553-560, 1977. [PubMed: 341373, related citations] [Full Text: Pubget]

5. Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., Fleming, M. D., Schreiber, S. L., Cantley, L. C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233, 2008. [PubMed: 18337823, related citations] [Full Text: Nature Publishing Group, Pubget]

6. Christofk, H. R., Vander Heiden, M. G., Wu, N., Asara, J. M., Cantley, L. C. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 452: 181-186, 2008. [PubMed: 18337815, related citations] [Full Text: Nature Publishing Group, Pubget]

7. David, C. J., Chen, M., Assanah, M., Canoll, P., Manley, J. L. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA spicing in cancer. Nature 463: 364-368, 2010. [PubMed: 20010808, related citations] [Full Text: Nature Publishing Group, Pubget]

8. Ikeda, Y., Noguchi, T. Allosteric regulation of pyruvate kinase M-2 isozyme involves a cysteine residue in the intersubunit contact. J. Biol. Chem. 273: 12227-12233, 1998. [PubMed: 9575171, related citations] [Full Text: HighWire Press, Pubget]

9. Junien, C., Rubinson-Skala, H., Dreyfus, J. C., Ravise, N., Boue, J., Boue, A., Kaplan, J. C. PK3: a new chromosome enzyme marker for gene dosage studies in chromosome 15 imbalance. Hum. Genet. 54: 191-196, 1980. [PubMed: 6930359, related citations] [Full Text: Pubget]

10. Kahn, A., Marie, J., Garreau, H., Sprengers, E. D. Subunit structure, interrelations and kinetic characteristics of the pyruvate kinase from erythrocytes and liver. Biochim. Biophys. Acta 523: 58-74, 1978.

11. Kitagawa, S., Obata, T., Hasumura, S., Pastan, I., Cheng, S.-Y. A cellular 3,3-prime,5-triiodo-L-thyronine binding protein from a human carcinoma cell line: purification and characterization. J. Biol. Chem. 262: 3903-3908, 1987. [PubMed: 3818670, related citations] [Full Text: HighWire Press, Pubget]

12. Levine, M., Muirhead, H., Stammers, D. K., Stuart, D. I. Structure of pyruvate kinase and similarities with other enzymes: possible implications for protein taxonomy and evolution. Nature 271: 626-630, 1978. [PubMed: 625331, related citations] [Full Text: Pubget]

13. Popescu, N. C., Cheng, S. Y. Chromosomal localization of the gene for a human cytosolic thyroid hormone binding protein homologous to the subunit of pyruvate kinase, subtype M(2). Somat. Cell Molec. Genet. 16: 593-598, 1990. [PubMed: 2267632, related citations] [Full Text: Pubget]

14. Ritter, H., Friedrichson, U., Schmitt, J. Genetic variation of mannose phosphate isomerase in man. Humangenetik 22: 261 only, 1974.

15. Roychoudhury, A. K., Nei, M. Human Polymorphic Genes: World Distribution. New York: Oxford Univ. Press (pub.) 1988.

16. Shows, T. B. Linkage of loci for human pyruvate kinase and mannosephosphate isomerase in somatic cell hybrids. (Abstract) Am. J. Hum. Genet. 24: 13A only, 1972.

17. Shows, T. B. Somatic cell genetics of enzyme markers associated with three human linkage groups.In: Davidson, R. L. : Proc. Conf. Somatic Cell Hybridization, Orlando, Fla. (pub.) 1973.

18. Takenaka, M., Noguchi, T., Sadahiro, S., Hirai, H., Yamada, K., Matsuda, T., Imai, E., Tanaka, T. Isolation and characterization of the human pyruvate kinase M gene. Europ. J. Biochem. 198: 101-106, 1991. [PubMed: 2040271, related citations] [Full Text: Blackwell Publishing, Pubget]

19. Tani, K., Yoshida, M. C., Satoh, H., Mitamura, K., Noguchi, T., Tanaka, T., Fujii, H., Miwa, S. Human M(2)-type pyruvate kinase: cDNA cloning, chromosomal assignment and expression in hepatoma. Gene 73: 509-516, 1988. [PubMed: 2854097, related citations] [Full Text: Pubget]

20. Tsutsumi, H., Tani, K., Fujii, H., Miwa, S. Expression of L- and M-type pyruvate kinase in human tissues. Genomics 2: 86-89, 1988. [PubMed: 2838416, related citations] [Full Text: Elsevier Science, Pubget]

21. Vander Heiden, M. G., Locasale, J. W., Swanson, K. D., Sharfi, H., Heffron, G. J., Amador-Noguez, D., Christofk, H. R., Wagner, G., Rabinowitz, J. D., Asara, J. M., Cantley, L. C. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329: 1492-1499, 2010. [PubMed: 20847263, related citations] [Full Text: HighWire Press, Pubget]

22. Van Heyningen, V., Bobrow, M., Bodmer, W. F., Gardiner, S. E., Povey, S., Hopkinson, D. A. Chromosome assignment of some human enzyme loci: mitochondrial malate dehydrogenase to 7, mannosephosphate isomerase and pyruvate kinase to 15 and probably, esterase D to 13. Ann. Hum. Genet. 38: 295-303, 1975. [PubMed: 1137344, related citations] [Full Text: Pubget]

23. Westerveld, A., Van Someren, H., Van Henegouwen, H. M. A., Oosterbaan, R. A. Synteny relationship between the human loci for hexosaminidase-A, mannose phosphate isomerase, and pyruvate kinase-3: studies in man-Chinese hamster somatic cell hybrids. Birth Defects Orig. Art. Ser. XI(3): 283-284, 1975. Note: Alternate: Cytogenet. Cell Genet. 14: 453-454, 1975.

24. Williams, J. M., Chen, G.-C., Zhu, L., Rest, R. F. Using the yeast two-hybrid system to identify human epithelial cell proteins that bind gonococcal Opa proteins: intracellular gonococci bind pyruvate kinase via their Opa proteins and require host pyruvate for growth. Molec. Microbiol. 27: 171-186, 1998.

25. Yang, W., Xia, Y., Ji, H., Zheng, Y., Liang, J., Huang, W., Gao, X., Aldape, K., Lu, Z. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature 480: 118-122, 2011. [PubMed: 22056988, related citations] [Full Text: Nature Publishing Group, Pubget]

Contributors: Ada Hamosh - updated : 1/4/2012
Ada Hamosh - updated : 11/2/2010
Ada Hamosh - updated : 2/18/2010
Ada Hamosh - updated : 5/21/2008
Patricia A. Hartz - updated : 5/5/2005
Paul J. Converse - updated : 6/13/2001
Creation Date: Victor A. McKusick : 6/2/1986
Edit History: alopez : 01/12/2012
terry : 1/4/2012
alopez : 11/8/2010
terry : 11/2/2010
alopez : 2/24/2010
alopez : 2/24/2010
terry : 2/18/2010
alopez : 5/22/2008
terry : 5/21/2008
carol : 11/18/2005
wwang : 6/30/2005
wwang : 6/23/2005
terry : 5/5/2005
carol : 7/17/2003
mgross : 6/15/2001
terry : 6/13/2001
dkim : 7/7/1998
mimadm : 2/25/1995
warfield : 4/21/1994
supermim : 3/16/1992
carol : 3/5/1992
carol : 9/11/1991
supermim : 3/20/1990