New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase

doi:10.1016/S0167-4838(99)00119-3

Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology

Volume 1432, Issue 2, 13 July 1999, Pages 159-184

Biochimica et Biophy...

https://doi.org/10.1016/S0167-4838(99)00119-3 Get rights and content

Abstract

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) was considered a classical glycolytic protein examined for its pivotal role in energy production. It was also used as a model protein for analysis of protein structure and enzyme mechanisms. The GAPDH gene was utilized as a prototype for studies of genetic organization, expression and regulation. However, recent evidence demonstrates that mammalian GAPDH displays a number of diverse activities unrelated to its glycolytic function. These include its role in membrane fusion, microtubule bundling, phosphotransferase activity, nuclear RNA export, DNA replication and DNA repair. These new activities may be related to the subcellular localization and oligomeric structure of GAPDH in vivo. Furthermore, other investigations suggest that GAPDH is involved in apoptosis, age-related neurodegenerative disease, prostate cancer and viral pathogenesis. Intriguingly, GAPDH is also a unique target of nitric oxide. This review discusses the functional diversity of GAPDH in relation to its protein structure. The mechanisms through which mammalian cells may utilize GAPDH amino acid sequences to provide these new functions and to determine its intracellular localization are considered. The interrelationship between new GAPDH activities and its role in cell pathologies is addressed.

Introduction

“Nature is nowhere accustomed more openly to display her secret mysteries than in the cases where she shows traces of her work apart from the beaten path.” William Harvey

The purpose of this review is to consider new, recent studies which suggest the need to reinterpret both the structure and the function of the protein glyceraldehyde-3-phosphate dehydrogenase (GAPDH, EC 1.2.1.12) in mammalian cells. For over three decades, GAPDH was studied for its pivotal role in glycolysis. As an abundant cell protein, it proved useful as a model for investigations examining basic mechanisms of enzyme action as well as the relationship between amino acid sequence and protein structure. Further, with the advent of molecular technology, GAPDH, as a putative ‘house-keeping’ gene, provided a model with which to use new methods for gene analysis to advance our understanding of the mechanisms through which cells organize and express their genetic information.

As with many things in life, what is thought to be simple and relatively straight-forward turns out to be quite complex and elaborate. In this regard, a number of studies, accelerating in the last decade [1], have indicated that GAPDH is not an uncomplicated, simple glycolytic protein. Instead, as illustrated in Fig. 1, independent laboratories identified diverse biological properties of the mammalian GAPDH protein. These included roles for GAPDH in membrane transport and in membrane fusion, microtubule assembly, nuclear RNA export, protein phosphotransferase/kinase reactions, the translational control of gene expression, DNA replication and DNA repair. Each activity appears to be distinct from its glycolytic function.

Other independent studies implicate GAPDH as an essential part of the program of gene expression observed in apoptosis and as part of the cellular phenotype of age-related neuronal disorders. In the former, this may include nuclear translocation of GAPDH into the nucleus without the induction of nuclear GAPDH glycolytic activity. In the latter, this may include the physical association of GAPDH with the β-amyloid precursor protein in Alzheimer’s disease and with proteins involved in ‘gain of function’ CAG triplet repeat disorders. Drugs which inhibit apoptosis and are currently in use to treat Parkinson’s disease specifically bind to GAPDH. Recent evidence also suggests a role for GAPDH in the etiology of prostate cancer. This may involve the dysregulation of GAPDH gene expression and the appearance of new GAPDH isoforms. Lastly, other laboratories have indicated a relationship between GAPDH and the pharmacology and toxicology of nitric oxide. NO induces oxidatively the covalent binding of NAD⁺ to GAPDH and, by S-nitrosylation, inhibits its dehydrogenase activity. At present, it does not appear that any other mammalian protein is so modified by nitric oxide.

Accordingly, the focus of this review is to consider the structure of the GAPDH protein as it relates to the new and novel functions identified for it in multiple reports from independent investigators. The basic rationale which will be followed is to discuss the functional diversity of GAPDH. Subsequently, reinterpretation of GAPDH protein structure will be addressed to postulate mechanisms through which classically defined GAPDH amino acid sequences may now be used in mammalian cells for such non-glycolytic activities. GAPDH genetic organization and protein structure will be discussed in relation to its role in fundamental biological processes (i.e., apoptosis) or pathologies (i.e., neuronal disorders). In addition, agents (i.e., nitric oxide, glutathione, the β-amyloid protein, the Huntington protein) which might affect GAPDH structure could dramatically alter its function. Considering its multidimensional nature, such alterations in GAPDH structure and function would induce pleiotropic changes in mammalian cells.

Section snippets

Functional diversity of mammalian GAPDH

The multidimensional nature of GAPDH is based on a series of new studies by independent laboratories. For the purposes of this section, these recent investigations will be grouped into two categories. The first group includes studies which identify new activities of GAPDH. As such, they provide documentation of specific functions apart from its conventional dehydrogenase activity. The second group includes new studies which identify the specific binding between GAPDH and cellular

Structure–function analysis of GAPDH: non-glycolytic activities

As described in the previous section, mammalian GAPDH exhibits a variety of functions distinct from its classical glycolytic dehydrogenase activity. In particular, the emerging understanding of its multifunctional activities, subcellular localization and potential role in apoptosis, neuronal disorders and prostate cancer requires new molecular studies evaluating its nucleotide and amino acid sequence as well as its protein–protein interactions in relation to its non-glycolytic functions.

Organization and expression of the mammalian GAPDH gene

In previous sections we discussed the multiple activities of mammalian GAPDH. We considered as well mechanisms through which its conventional glycolytic structure may have been adapted to these new functions. In this section, we intend to first review the genetic organization and expression of mammalian GAPDH. Second, we will then introduce studies which present an apparent paradox with respect to the interrelationship between GAPDH gene structure and its functional diversity.

Nitric oxide/GAPDH interactions

Nitric oxide exhibits a duality of function in mammalian cells. First, it is a critical intracellular compound which functions as an in vivo messenger within a number of cell processes including inflammation, the immune response and acts as a neurotransmitter (reviewed in [122], [123]). Initial studies identified cGMP-dependent pathways mediated by guanylate cyclase as basic molecular mechanisms for NO function. Other studies indicated a role for cGMP independent pathways in the mechanisms of

Role of GAPDH in apoptosis

Initial studies in cerebral granular cells (CGCs) first demonstrated the role of GAPDH in apoptosis [139], [140], [141], [142], [143]. CGCs in culture underwent apoptosis at approximately 17 days in vitro (DIV). SDS–PAGE analysis revealed the appearance of a 38 kDa protein coordinate with the induction of apoptosis. Actinomycin D and cycloheximide reduced expression of the unknown protein. N-Terminal sequence analysis identified the protein as GAPDH. The physiological relevance of GAPDH

GAPDH and neurodegenerative disease: protein–protein interactions

As indicated above, recent studies provide significant evidence for the role of GAPDH in apoptosis. GAPDH participation in this basic cellular process may be interrelated with its role in human pathology. This is suggested by several independent studies which indicate a specific relationship in vivo between GAPDH and a number of proteins directly related to the pathology of age-related human neuronal disorders. These include specific protein–protein interactions between GAPDH and the β-amyloid

GAPDH and prostate cancer

Investigations on the role of GAPDH in the cellular phenotype of prostate cancer focused on alterations of GAPDH gene and protein expression. In these studies prostate cancer cell lines as well as prostate tissue were examined. The rationale was that, were GAPDH to play a role in prostate cancer, it would be reasonable to detect transcriptional or translational aberrations as compared to normal cells.

Initial studies quantitated GAPDH mRNA levels in rat adenocarcinoma cell lines in comparison

Conclusions

The state of our knowledge with respect to the functional diversity of mammalian GAPDH and the underlying basic mechanisms which provide for its multidimensional nature is still in its infancy. It may be accurate to say that there are many questions which may be posed with respect to GAPDH structure and function. It is also clear that few answers are currently available to respond to those queries. Accordingly, fertile ground exists for future experimentation. Several areas appear promising.

Acknowledgements

The generous assistance of Dr. Jerome L. Gabriel in molecular modeling analysis is gratefully acknowledged. Work in the author’s laboratory was funded by a grant from the National Institute on Aging (AG14566).

References (166)

J.A Kant et al.
Specificity in the association of glyceraldehyde 3-phosphate dehydrogenase with isolated human erythrocyte membranes
J. Biol. Chem.
(1973)
C.F McDaniel et al.
The interaction of glyceraldehyde 3-phosphate dehydrogenase with human erythrocyte membranes
J. Biol. Chem.
(1974)
H.J Kliman et al.
Association of glyceraldehyde-3-phosphate dehydrogenase with the human red cell membrane: a kinetic analysis
J. Biol. Chem.
(1980)
I.-H Tsai et al.
Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase
J. Biol. Chem.
(1982)
R.W Allen et al.
Reorientation of membrane polypeptides during erythrocyte maturation
Blood
(1983)
R.W Allen et al.
Identification of the 37-kDa protein displaying a variable interaction with the erythroid cell membrane as glyceraldehyde-3-phosphate dehydrogenase
J. Biol. Chem.
(1987)
A.E Lopez Vinals et al.
Characterization of the fusogenic properties of glyceraldehyde-3-phosphate dehydrogenase: fusion of phospholipid vesicles
Biochem. Biophys. Res. Commun.
(1987)
X Han et al.
Reconstitution of membrane fusion between pancreatic islet secretory granules and plasma membranes: catalysis by a protein constituent recognized by monoclonal antibodies directed against glyceraldehyde-3-phosphate dehydrogenase
Biochim. Biophys. Acta
(1998)
A.H Caswell et al.
Interaction of glyceraldehyde-3-phosphate dehydrogenase with isolated microsomal subfractions of skeletal muscle
J. Biol. Chem.
(1985)
J.L Walsh et al.
Glycolytic enzyme interactions with tubulin and microtubules
Biochim. Biophys. Acta
(1989)

J.F Launay et al.

Glyceraldehyde-3-phosphate dehydrogenase is a microtubule binding protein in a human colon tumor cell line

Biochim. Biophys. Acta

(1989)

K.W Volker et al.

Glycolytic enzymes and assembly of microtubule networks

Comp. Biochem. Physiol.

(1995)

K.W Volker et al.

A glycolytic enzyme binding domain on tubulin

Arch. Biochem. Biophys.

(1997)

C Durrieu et al.

Microtubules bind glyceraldehyde 3-phosphate dehydrogenase and modulate its enzyme activity and quaternary structure

Arch. Biochem. Biophys.

(1987)

V.I Muronetz et al.

Binding constants and stoichiometries of glyceraldehyde 3-phosphate dehydrogenase-tubulin complexes

Arch. Biochem. Biophys.

(1994)

S.M Constantinides et al.

Reversible dissociation of tetrameric rabbit muscle glyceraldehyde 3-phosphate dehydrogenase into trimers and monomers by adenosine triphosphate

J. Biol. Chem.

(1969)

M Oguchi et al.

Regulation of glyceraldehyde 3-phosphate dehydrogenase by phosphocreatine and adenosine triphosphate. IV. Factors affecting in vivo control of enzymatic activity

J. Biol. Chem.

(1973)

M Engel et al.

Glyceraldehyde-3-phosphate dehydrogenase and Nm23-H1/nucleoside diphosphate kinase A: two old enzymes combine for the novel Nm23 protein phosphotransferase function

J. Biol. Chem.

(1998)

L.I Ashmarina et al.

Phosphorylation of D-glyceraldehyde-3-phosphate dehydrogenase by Ca²⁺/calmodulin-dependent protein kinase II

FEBS Lett.

(1988)

E.A Sergienko et al.

D-glyceraldehyde-3-phosphate dehydrogenase purified from rabbit muscle contains phosphotyrosine

FEBS Lett.

(1992)

W.-Q Zang et al.

Identification of glyceraldehyde-3-phosphate as a cellular protein that binds to the hepatitis B virus posttranscriptional regulatory element

Virology

(1998)

S.E McNulty et al.

Transcriptional regulation of glyceraldehyde-3-phosphate dehydrogenase by 2,3,7,8-tetrachlorodibenzo-p-dioxin

Biochem. Biophys. Res. Commun.

(1995)

A.G Ryazanov

Glyceraldehyde-3-phosophate dehydrogenase is one of the three major RNA-binding proteins of rabbit reticulocytes

FEBS Lett.

(1985)

E Nagy et al.

Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD⁺-binding region (Rossman Fold)

J. Biol. Chem.

(1995)

B.P De et al.

Specific interaction in vitro and in vivo of glyceraldehyde-3-phosphate dehydrogenase and LA protein with cis-acting RNAs of human parainfluenza virus type 3

J. Biol. Chem.

(1996)

D.E Schultz et al.

Specific interaction of glyceraldehyde-3-phosphate dehydrogenase with the 5′-nontranslated RNA of hepatitis A virus

J. Biol. Chem.

(1996)

R.L Karpel et al.

A basic isozyme of yeast glyceraldehyde-3-phosphate dehydrogenase with nucleic acid helix-destabilizing activity

Biochim. Biophys. Acta

(1981)

M Sioud et al.

Enhancement of hammerhead ribozyme catalysis by glyceraldehyde-3-phosphate dehydrogenase

J. Mol. Biol.

(1996)

L Gasmi et al.

The diadenosine polyphosphates, Ap₃A and Ap₄A and adenosine triphosphate interact with granulocyte-macrophage colony-stimulating factor to delay neutrophil apoptosis: Implications for neutrophil:plated interactions during inflammation

Blood

(1996)

A Vartanian et al.

Opposite effects of cell differentiation and apoptosis on Ap₃A/Ap₄A ratio in human cell cultures

FEBS Lett.

(1997)

C Lind et al.

Studies on the mechanism of oxidative modification of human glyceraldehyde-3-phosphate dehydrogenase by glutathione: Catalysis by glutaredoxin

Biochem. Biophys. Res. Commun.

(1998)

M Puder et al.

Glutathione conjugates recognize the Rossman fold of glyceraldehyde-3-phosphate dehydrogenase

J. Biol. Chem.

(1997)

Z Zhao et al.

Reduced glutathione prevents nitric oxide-induced apoptosis in vascular smooth muscle cells

Biochim. Biophys. Acta

(1997)

P Froissard et al.

Role of glutathione metabolism in the glutamate-induced programmed cell death of neuronal-like PC12 cells

Eur. J. Pharmacol.

(1997)

S.E Boggs et al.

Glutathione levels determine apoptosis in macrophages

Biochem. Biophys. Res. Commun.

(1998)

M.R.N Murthy et al.

Structure of lobster apo-d-glyceraldehyde-3-phosphate dehydrogenase at 3.0 A resolution

J. Mol. Biol.

(1980)

A.G Leslie et al.

Coenzyme binding in crystals of glyceraldehyde-3-phosphate dehydrogenase

J. Mol. Biol.

(1983)

J.P Griffith et al.

Molecular symmetry of glyceraldehyde-3-phosphate dehydrogenase from Bacillus coagulans

J. Mol. Biol.

(1983)

W.D Mercer et al.

Twinning in crystals of human skeletal muscle D-glyceraldehyde-3-phosphate dehydrogenase

J. Mol. Biol.

(1976)

M.A Holmes et al.

Crystallographic data for sturgeon holo-D-glyceraldehyde-3-phosphate dehydrogenase: a holo-D-glyceraldehyde-3-phosphate dehydrogenase with crystallographic 2-fold symmetry

J. Mol. Biol.

(1977)

J.L Gabriel et al.

Molecular modeling of phytochrome

J. Theor. Biol.

(1991)

D Moras et al.

Studies of asymmetry in the three-dimensional structure of lobster d-glyceraldehyde-3-phosphate dehydrogenase

J. Biol. Chem.

(1975)

J Ovadi et al.

SH groups masked by subunit interaction in glyceraldehyde-3-phosphate dehydrogenase

Biochim. Biophys. Acta

(1973)

K.W Olsen et al.

Sequence variability and structure of D-glyceraldehyde-3-phosphate dehydrogenase

J. Biol. Chem.

(1975)

D Eby et al.

Role of lysine residues in the binding of glyceraldehyde-3-phosphate dehydrogenase to human erythrocyte membranes

Biochem. Biophys. Res. Commun.

(1983)

C Dingwall et al.

Nuclear targeting sequences – a consensus

Trends Biochem. Sci.

(1991)

K Meyer-Siegler et al.

A human nuclear uracil DNA glycosylase is the 37 kDa subunit of glyceraldehyde-phosphate dehydrogenase

Proc. Natl. Acad. Sci. USA

(1991)

M.J.A Tanner et al.

The isolation and functional identification of a protein from the human erythrocyte ‘ghost’

Biochem. J.

(1971)

M.S Wooster et al.

Adsorption of glyceraldehyde 3-phosphate dehydrogenase on condensed monolayers of phospholipid

Biochem. J.

(1976)

J Yu et al.

Associations of Band 3, the predominant polypeptide of the human erythrocyte membrane

J. Biol. Chem.

(1975)

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ReviewNew insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase

Abstract

Introduction

Section snippets

Functional diversity of mammalian GAPDH

Structure–function analysis of GAPDH: non-glycolytic activities

Organization and expression of the mammalian GAPDH gene

Nitric oxide/GAPDH interactions

Role of GAPDH in apoptosis

GAPDH and neurodegenerative disease: protein–protein interactions

GAPDH and prostate cancer

Conclusions

Acknowledgements

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Blood

J. Biol. Chem.

Biochem. Biophys. Res. Commun.

Biochim. Biophys. Acta

J. Biol. Chem.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Comp. Biochem. Physiol.

Arch. Biochem. Biophys.

Arch. Biochem. Biophys.

Arch. Biochem. Biophys.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

FEBS Lett.

FEBS Lett.

Virology

Biochem. Biophys. Res. Commun.

FEBS Lett.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Biochim. Biophys. Acta

J. Mol. Biol.

Blood

FEBS Lett.

Biochem. Biophys. Res. Commun.

J. Biol. Chem.

Biochim. Biophys. Acta

Eur. J. Pharmacol.

Biochem. Biophys. Res. Commun.

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

J. Theor. Biol.

J. Biol. Chem.

Biochim. Biophys. Acta

J. Biol. Chem.

Biochem. Biophys. Res. Commun.

Trends Biochem. Sci.

A human nuclear uracil DNA glycosylase is the 37 kDa subunit of glyceraldehyde-phosphate dehydrogenase

Proc. Natl. Acad. Sci. USA

The isolation and functional identification of a protein from the human erythrocyte ‘ghost’

Biochem. J.

Adsorption of glyceraldehyde 3-phosphate dehydrogenase on condensed monolayers of phospholipid

Biochem. J.

Associations of Band 3, the predominant polypeptide of the human erythrocyte membrane

J. Biol. Chem.

Review
New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase