Glucose-6-phosphate isomerase

Not to be confused with D-xylose isomerase.
Glucose-6-phosphate isomerase
Identifiers
EC number 5.3.1.9
CAS number 9001-41-6
Databases
IntEnz IntEnz view
BRENDA BRENDA entry
ExPASy NiceZyme view
KEGG KEGG entry
MetaCyc metabolic pathway
PRIAM profile
PDB structures RCSB PDB PDBe PDBsum
Gene Ontology AmiGO / EGO
Bacterial phospho-glucose isomerase C-terminal region

crystal structure of phosphoglucose/phosphomannose isomerase from pyrobaculum aerophilum in complex with fructose 6-phosphate
Identifiers
Symbol bact-PGI_C
Pfam PF10432
InterPro IPR019490
CDD cd05016
Phosphoglucose isomeras
Identifiers
Symbol PGI
Pfam PF00342
SCOP 1pgi
SUPERFAMILY 1pgi
CDD cd05015
Glucose-6-phosphate isomerase

PDB rendering based on 1dqr.
Available structures
PDB Ortholog search: PDBe, RCSB
Identifiers
Symbols GPI ; AMF; GNPI; NLK; PGI; PHI; SA-36; SA36
External IDs OMIM: 172400 MGI: 95797 HomoloGene: 145 GeneCards: GPI Gene
EC number 5.3.1.9
RNA expression pattern
More reference expression data
Orthologs
Species Human Mouse
Entrez 2821 14751
Ensembl ENSG00000105220 ENSMUSG00000036427
UniProt P06744 P06745
RefSeq (mRNA) NM_000175 NM_008155
RefSeq (protein) NP_000166 NP_032181
Location (UCSC) Chr 19:
34.36 – 34.4 Mb
Chr 7:
34.2 – 34.23 Mb
PubMed search

Glucose-6-phosphate isomerase (GPI), alternatively known as phosphoglucose isomerase (PGI) or phosphohexose isomerase (PHI), is an enzyme that in humans is encoded by the GPI gene on chromosome 19.[1] This gene encodes a member of the glucose phosphate isomerase protein family. The encoded protein has been identified as a moonlighting protein based on its ability to perform mechanistically distinct functions. In the cytoplasm, the gene product functions as a glycolytic enzyme (glucose-6-phosphate isomerase) that interconverts glucose-6-phosphate (G6P) and fructose-6-phosphate (F6P). Extracellularly, the encoded protein (also referred to as neuroleukin) functions as a neurotrophic factor that promotes survival of skeletal motor neurons and sensory neurons, and as a lymphokine that induces immunoglobulin secretion. The encoded protein is also referred to as autocrine motility factor (AMF) based on an additional function as a tumor-secreted cytokine and angiogenic factor. Defects in this gene are the cause of nonspherocytic hemolytic anemia, and a severe enzyme deficiency can be associated with hydrops fetalis, immediate neonatal death and neurological impairment. Alternative splicing results in multiple transcript variants. [provided by RefSeq, Jan 2014][2]

Structure

Functional GPI is a 64-kDa dimer composed of two identical monomers.[3][4] The two monomers interact notably through the two protrusions in a hugging embrace. The active site of each monomer is formed by a cleft between the two domains and the dimer interface.[3]

GPI monomers are made of two domains, one made of two separate segments called the large domain and the other made of the segment in between called the small domain.[5] The two domains are each αβα sandwiches, with the small domain containing a five-strand β-sheet surrounded by α-helices while the large domain has a six-stranded β-sheet.[3] The large domain, located at the N-terminal, and the C-terminal of each monomer also contain "arm-like" protrusions.[5][6] Several residues in the small domain serve to bind phosphate, while other residues, particularly His388, from the large and C-terminal domains are crucial to the sugar ring-opening step catalyzed by this enzyme. Since the isomerization activity occurs at the dimer interface, the dimer structure of this enzyme is critical to its catalytic function.[6]

It is hypothesized that serine phosphorylation of this protein induces a conformational change to its secretory form.[4]

Mechanism

The mechanism that GPI uses to interconvert glucose 6-phosphate and fructose 6-phosphate consists of three major steps: opening the glucose ring, isomerizing glucose into fructose through an enediol intermediate, and closing the fructose ring.[7]

Isomerization of glucose

D-Glucose Phosphoglucose isomerase D-Fructose
 
 
  Phosphoglucose isomerase
α-D-Glucose 6-phosphate Phosphoglucose isomerase β-D-Fructose 6-phosphate
 
 
  Phosphoglucose isomerase

Compound C00668 at KEGG Pathway Database. Enzyme 5.3.1.9 at KEGG Pathway Database. Compound C05345 at KEGG Pathway Database. Reaction R00771 at KEGG Pathway Database.

Glucose 6 phosphate binds to GPI as a hemiacetal ring. The ring is opened in a "push-pull" mechanism by His388, which protonates the C5 oxygen, and Lys518, which deprotonates the C1 hydroxyl group. This creates an open chain aldose. Then, the substrated is rotated about the C3-C4 bond to position it for isomerization. At this point, Glu357 deprotonates C2 to create a cis-enediolate intermediate stabilized by Arg272. To complete the isomerization, Glu357 donates its proton to C1, the C2 hydroxyl group loses its proton and the open-chain ketose, Fructose 6-phosphate is formed. Finally, the ring is closed by rotating the substrate about the C3-C4 bond again and deptrotonating the C5 hydroxyl with Lys518 to cause to the opposite of the ring opening mechanism used to start the reaction.[8]

Function

This gene belongs to the GPI family.[2] The protein encoded by this gene is a dimeric enzyme that catalyzes the reversible isomerization of G6P and F6P.[9][10] Since the reaction is reversible, its direction is determined by G6P and F6P concentrations.[6]

glucose 6-phosphate <=> fructose 6-phosphate

The protein has different functions inside and outside the cell. In the cytoplasm, the protein is involved in glycolysis and gluconeogenesis, as well as the pentose phosphate pathway.[6] Outside the cell, it functions as a neurotrophic factor for spinal and sensory neurons, called neuroleukin.[10] The same protein is also secreted by cancer cells, where it is called autocrine motility factor[11] and stimulates metastasis.[12] Extracellular GPI is also known to function as a maturation factor.[6][10]

Neuroleukin

Though originally treated as separate proteins, cloning technology demonstrated that GPI is almost identical to the protein neuroleukin.[13] Neuroleukin is a neurotrophic factor for spinal and sensory neurons. It is found in large amounts in muscle, brain, heart, and kidneys.[14] Neuroleukin also acts as a lymphokine secreted by T cells stimulated by lectin. It induces immunoglobulin secretion in B cells as part of a response that activates antibody-secreting cells.[15]

Autocrine Motility Factor

Cloning experiments also revealed that GPI is identical to the protein known as autocrine motility factor (AMF).[16] AMF produced and secreted by cancer cells and stimulates cell growth and motility as a growth factor.[17] AMF is thought to play a key role in cancer metastasis by activating the MAPK/ERK or PI3K/AKT pathways.[18][19][20] In the PI3K/AKT pathway, AMF interacts with gp78/AMFR to regulate ER calcium release, and therefore protect against apoptosis in response to ER stress.[18]

Prokaryotic bifunctional glucose-6-phosphate isomerase

In some archaea and bacteria glucose-6-phosphate isomerase activity occurs via a bifunctional enzyme that also exhibits phosphomannose isomerase (PMI) activity. Though not closely related to eukaryotic GPIs, the bifunctional enzyme is similar enough that the sequence includes the cluster of threonines and serines that forms the sugar phosphate-binding site in conventional GPI. The enzyme is thought to use the same catalytic mechanisms for both glucose ring-opening and isomerisation for the interconversion of G6P to F6P.[21]

Clinical significance

A deficiency of GPI is responsible for 4% of the hemolytic anemias due to glycolytic enzyme deficiencies.[9][10][22][23] Several cases of GPI deficiency have recently been identified.[24]

Elevated serum GPI levels have been used as a prognostic biomarker for colorectal, breast, lung, kidney, gastrointestinal, and other cancers.[4][10] As AMF, GPI is attributed with regulating cell migration during invasion and metastasis.[4] One study showed that the external layers of breast tumor spheroids (BTS) secrete GPI, which induces epithelial–mesenchymal transition (EMT), invasion, and metastasis in BTS. The GPI inhibitors ERI4P and 6PG were found to block metastasis of BTS but not BTS glycolysis or fibroblast viability. In addition, GPI is secreted exclusively by tumor cells and not normal cells. For these reasons, GPI inhibitors may be a safer, more targeted approach for anti-cancer therapy.[25] GPI also participates in a positive feedback loop with HER2, a major breast cancer therapeutic target, as GPI enhances HER2 expression and HER2 overexpression enhances GPI expression, and so on. As a result, GPI activity likely confers resistance in breast cancer cells against HER2-based therapies using Herceptin/Trastuzumab, and should be considered as an additional target when treating patients.[20]

Interactions

GPI is known to interact with:

Interactive pathway map

Click on genes, proteins and metabolites below to link to respective articles. [§ 1]

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GlycolysisGluconeogenesis_WP534 go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to article go to Entrez go to article go to article go to article go to article go to article go to WikiPathways go to article go to Entrez go to article

|{{{bSize}}}px|alt=Glycolysis and Gluconeogenesis edit]]

Glycolysis and Gluconeogenesis edit

  1. The interactive pathway map can be edited at WikiPathways: "GlycolysisGluconeogenesis_WP534".

References

  1. "UniProtKB: P06744 (G6PI_HUMAN)".
  2. 1 2 "Entrez Gene: GPI glucose phosphate isomerase".
  3. 1 2 3 Jeffery CJ, Bahnson BJ, Chien W, Ringe D, Petsko GA (February 2000). "Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine motility factor, and differentiation mediator". Biochemistry 39 (5): 955–64. doi:10.1021/bi991604m. PMID 10653639.
  4. 1 2 3 4 Haga A, Niinaka Y, Raz A (2000). "Phosphohexose isomerase/autocrine motility factor/neuroleukin/maturation factor is a multifunctional phosphoprotein.". Biochim. Biophys. Acta 1480 (1-2): 235–44. doi:10.1016/s0167-4838(00)00075-3. PMID 11004567.
  5. 1 2 Sun YJ, Chou CC, Chen WS, Wu RT, Meng M, Hsiao CD (May 1999). "The crystal structure of a multifunctional protein: phosphoglucose isomerase/autocrine motility factor/neuroleukin". Proc Natl Acad Sci U S A 96 (10): 5412–5417. doi:10.1073/pnas.96.10.5412. PMC 21873. PMID 10318897.
  6. 1 2 3 4 5 Cordeiro, AT; Godoi, PH; Silva, CH; Garratt, RC; Oliva, G; Thiemann, OH (21 February 2003). "Crystal structure of human phosphoglucose isomerase and analysis of the initial catalytic steps.". Biochimica et Biophysica Acta 1645 (2): 117–22. doi:10.1016/s1570-9639(02)00464-8. PMID 12573240.
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  24. "GPI Deficiency".
  25. Gallardo-Pérez, JC; Rivero-Segura, NA; Marín-Hernández, A; Moreno-Sánchez, R; Rodríguez-Enríquez, S (June 2014). "GPI/AMF inhibition blocks the development of the metastatic phenotype of mature multi-cellular tumor spheroids.". Biochimica et Biophysica Acta 1843 (6): 1043–53. doi:10.1016/j.bbamcr.2014.01.013. PMID 24440856.

Further reading

  • Walker JI, Faik P, Morgan MJ (1990). "Characterization of the 5' end of the gene for human glucose phosphate isomerase (GPI).". Genomics 7 (4): 638–43. doi:10.1016/0888-7543(90)90212-D. PMID 2387591. 
  • Brownstein BH, Silverman GA, Little RD, et al. (1989). "Isolation of single-copy human genes from a library of yeast artificial chromosome clones.". Science 244 (4910): 1348–51. doi:10.1126/science.2544027. PMID 2544027. 
  • Mizrachi Y (1989). "Neurotrophic activity of monomeric glucophosphoisomerase was blocked by human immunodeficiency virus (HIV-1) and peptides from HIV-1 envelope glycoprotein.". J. Neurosci. Res. 23 (2): 217–24. doi:10.1002/jnr.490230212. PMID 2547084. 
  • Gurney ME, Apatoff BR, Spear GT, et al. (1986). "Neuroleukin: a lymphokine product of lectin-stimulated T cells.". Science 234 (4776): 574–81. doi:10.1126/science.3020690. PMID 3020690. 
  • Faik P, Walker JI, Redmill AA, Morgan MJ (1988). "Mouse glucose-6-phosphate isomerase and neuroleukin have identical 3' sequences.". Nature 332 (6163): 455–7. doi:10.1038/332455a0. PMID 3352745. 
  • Zanella A, Izzo C, Rebulla P, et al. (1981). "The first stable variant of erythrocyte glucose-phosphate isomerase associated with severe hemolytic anemia.". Am. J. Hematol. 9 (1): 1–11. doi:10.1002/ajh.2830090102. PMID 7435496. 
  • Faik P, Walker JI, Morgan MJ (1994). "Identification of a novel tandemly repeated sequence present in an intron of the glucose phosphate isomerase (GPI) gene in mouse and man.". Genomics 21 (1): 122–7. doi:10.1006/geno.1994.1233. PMID 7545951. 
  • Xu W, Beutler E (1995). "The characterization of gene mutations for human glucose phosphate isomerase deficiency associated with chronic hemolytic anemia.". J. Clin. Invest. 94 (6): 2326–9. doi:10.1172/JCI117597. PMC 330061. PMID 7989588. 
  • Xu W, Lee P, Beutler E (1996). "Human glucose phosphate isomerase: exon mapping and gene structure.". Genomics 29 (3): 732–9. doi:10.1006/geno.1995.9944. PMID 8575767. 
  • Baronciani L, Zanella A, Bianchi P, et al. (1996). "Study of the molecular defects in glucose phosphate isomerase-deficient patients affected by chronic hemolytic anemia.". Blood 88 (6): 2306–10. PMID 8822952. 
  • Beutler E, West C, Britton HA, et al. (1998). "Glucosephosphate isomerase (GPI) deficiency mutations associated with hereditary nonspherocytic hemolytic anemia (HNSHA).". Blood Cells Mol. Dis. 23 (3): 402–9. doi:10.1006/bcmd.1997.0157. PMID 9446754. 
  • Kanno H, Fujii H, Miwa S (1998). "Expression and enzymatic characterization of human glucose phosphate isomerase (GPI) variants accounting for GPI deficiency.". Blood Cells Mol. Dis. 24 (1): 54–61. doi:10.1006/bcmd.1998.0170. PMID 9616041. 
  • Kugler W, Breme K, Laspe P, et al. (1998). "Molecular basis of neurological dysfunction coupled with haemolytic anaemia in human glucose-6-phosphate isomerase (GPI) deficiency.". Hum. Genet. 103 (4): 450–4. doi:10.1007/s004390050849. PMID 9856489. 
  • Belyaeva OV, Balanovsky OP, Ashworth LK, et al. (1999). "Fine mapping of a polymorphic CA repeat marker on human chromosome 19 and its use in population studies.". Gene 230 (2): 259–66. doi:10.1016/S0378-1119(99)00056-6. PMID 10216265. 
  • Yakirevich E, Naot Y (2000). "Cloning of a glucose phosphate isomerase/neuroleukin-like sperm antigen involved in sperm agglutination.". Biol. Reprod. 62 (4): 1016–23. doi:10.1095/biolreprod62.4.1016. PMID 10727272. 
  • Haga A, Niinaka Y, Raz A (2000). "Phosphohexose isomerase/autocrine motility factor/neuroleukin/maturation factor is a multifunctional phosphoprotein.". Biochim. Biophys. Acta 1480 (1-2): 235–44. doi:10.1016/s0167-4838(00)00075-3. PMID 11004567. 

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