The SLC37 family of sugar-phosphate/phosphate exchangers

Current Topics in Membranes

Volumn 73, Issue , 2014, Pages 357-382

  Chou, Janice Y ^a   Mansfield, Brian C ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b Foundation Fighting Blindness   (United States)

Author keywords

Chlorogenic acid; Endoplasmic reticulum; Glucose 6 phosphate transporter; Glycogen storage disease type Ib

Indexed keywords

CARRIER PROTEIN; PHOSPHATE;

AMINO ACID SEQUENCE; ANIMAL; CARBOHYDRATE METABOLISM; CELL MEMBRANE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; CARBOHYDRATE METABOLISM; CELL MEMBRANE; HUMANS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHATES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84898648095     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800223-0.00010-4     Document Type: Chapter

References (67)

1. Almqvist J., Huang Y., Hovmöller S., Wang D.N. Homology modeling of the human microsomal glucose 6-phosphate transporter explains the mutations that cause the glycogen storage disease type Ib. Biochemistry 2004, 43(29):9289-9297.
2. Annabi B., Hiraiwa H., Mansfield B.C., Lei K.-J., Ubagai T., Polymeropoulos M.H., et al. The gene for glycogen storage disease type 1b maps to chromosome 11q23. American Journal of Human Genetics 1998, 62(2):400-405.
3. Arion W.J., Canfield W.K., Ramos F.C., Su M.L., Burger H.J., Hemmerle H., et al. Chlorogenic acid analogue S 3483: A potent competitive inhibitor of the hepatic and renal glucose-6-phosphatase systems. Achieves of Biochemistry and Biophysics 1998, 351(2):279-285.
4. Arion W.J., Lange A.J., Ballas L.M. Quantitative aspects of relationship between glucose 6-phosphate transport and hydrolysis for liver microsomal glucose-6-phosphatase system. Selective thermal inactivation of catalytic component in situ at acid pH. Journal of Biological Chemistry 1976, 251(16):6784-6790.
5. Arion W.J., Wallin B.K., Carlson P.W., Lange A.J. The specificity of glucose 6-phosphatase of intact liver microsomes. Journal of Biological Chemistry 1972, 247(8):2558-2565.
6. Bandsma R.H., Wiegman C.H., Herling A.W., Burger H.J., ter Harmsel A., Meijer A.J., et al. Acute inhibition of glucose-6-phosphate translocator activity leads to increased de novo lipogenesis and development of hepatic steatosis without affecting VLDL production in rats. Diabetes 2001, 50(11):2591-2597.
7. Bartoloni L., Antonarakis S.E. The human sugar-phosphate/phosphate exchanger family SLC37. Pflügers Archiv 2004, 447(5):780-783.
8. Bartoloni L., Wattenhofer M., Kudoh J., Berry A., Shibuya K., Kawasaki K., et al. Cloning and characterization of a putative human glycerol 3-phosphate permease gene (SLC37A1 or G3PP) on 21q22.3: Mutation analysis in two candidate phenotypes, DFNB10 and a glycerol kinase deficiency. Genomics 2000, 70(2):190-200.
9. Boztug K., Appaswamy G., Ashikov A., Schäffer A.A., Salzer U., Diestelhorst J., et al. A syndrome with congenital neutropenia and mutations in G6PC3. New England Journal of Medicine 2009, 360(1):32-43.
10. Caramelo J.J., Parodi A.J. How sugars convey information on protein conformation in the endoplasmic reticulum. Seminars in Cell and Developmental Biology 2007, 18(6):732-742.
11. Chen L.-Y., Lin B., Pan C.-J., Hiraiwa H., Chou J.Y. Structural requirements for the stability and microsomal transport activity of the human glucose-6-phosphate transporter. Journal of Biological Chemistry 2000, 275(44):34280-34286.
12. Chen S.Y., Pan C.J., Lee S., Peng W., Chou J.Y. Functional analysis of mutations in the glucose-6-phosphate transporter that cause glycogen storage disease type Ib. Molecular Genetics and Metabolism 2008, 95(4):220-223.
13. Chen S.Y., Pan C.J., Nandigama K., Mansfield B.C., Ambudkar S.V., Chou J.Y. The glucose-6-phosphate transporter is a phosphate-linked antiporter deficient in glycogen storage disease type Ib and Ic. FASEB Journal 2008, 22(7):2206-2213.
14. Chen L.-Y., Pan C.-J., Shieh J.-J., Chou J.Y. Structure-function analysis of the glucose-6-phosphate transporter deficient in glycogen storage disease type Ib. Human Molecular Genetics 2002, 11(25):3199-3207.
15. Chen L.-Y., Shieh J.-J., Lin B., Pan C.-J., Gao J.-L., Murphy P.M., et al. Impaired glucose homeostasis, neutrophil trafficking and function in mice lacking the glucose-6-phosphate transporter. Human Molecular Genetics 2003, 12(19):2547-2558.
16. Cheung Y.Y., Kim S.Y., Yiu W.H., Pan C.J., Jun H.S., Ruef R.A., et al. Impaired neutrophil activity and increased susceptibility to bacterial infection in mice lacking glucose-6-phosphatase-beta. Journal of Clinical Investigation 2007, 117(3):784-793.
17. Chou J.Y., Jun H.S., Mansfield B.C. Neutropenia in type Ib glycogen storage disease. Current Opinion in Hematology 2010, 17(1):36-42.
18. Chou J.Y., Jun H.S., Mansfield B.C. Glycogen storage disease type I and G6Pase-β deficiency: Etiology and therapy. Nature Reviews. Endocrinology 2010, 6(12):676-688.
19. Chou J.Y., Jun H.S., Mansfield B.C. The SLC37 family of phosphate-linked sugar phosphate antiporters. Molecular Aspects of Medicine 2013, 34(2-3):601-611.
20. Chou J.Y., Matern D., Mansfield B.C., Chen Y.-T. Type I glycogen storage diseases: Disorders of the glucose-6-phosphatase complex. Current Molecular Medicine 2002, 2(12):121-143.
21. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 1988, 16(22):10881-10890.
22. Dissanayake V.H., Jayasinghe J.D., Thilakaratne V., Jayasekara R.W. A novel mutation in SLC37A4 gene in a Sri Lankan boy with glycogen storage disease type Ib associated with very early onset neutropenia. Journal of Molecular and Genetic Medicine: An International Journal of Biomedical Research 2011, 5:262-263.
23. Fann M.C., Davies A.H., Varadhachary A., Kuroda T., Sevier C., Tsuchiya T., et al. Identification of two essential arginine residues in UhpT, the sugar phosphate antiporter of Escherichia coli. Journal of Membrane Biology 1998, 164(2):187-195.
24. Galli L., Orrico A., Marcolongo P., Fulceri R., Burchell A., Melis D., et al. Mutations in the glucose-6-phosphate transporter (G6PT) gene in patients with glycogen storage diseases type 1b and 1c. FEBS Letters 1999, 459(2):255-258.
25. Gerin I., Veiga-da-Cunha M., Achouri Y., Collet J.F., Van Schaftingen E. Sequence of a putative glucose-6-phosphate translocase, mutated in glycogen storage disease type 1b. FEBS Letters 1997, 419(2-3):235-238.
26. Gerin I., Veiga-da-Cunha M., Noel G., Van Schaftingen E. Structure of the gene mutated in glycogen storage disease type Ib. Gene 1999, 227(2):189-195.
27. Ghosh A., Shieh J.-J., Pan C.-J., Chou J.Y. Histidine-167 is the phosphate acceptor in glucose-6-phosphatase-β forming a phosphohistidine-enzyme intermediate during catalysis. Journal of Biological Chemistry 2004, 279(13):12479-12483.
28. 176 is the nucleophile forming the phosphohistidine-enzyme intermediate during catalysis. Journal of Biological Chemistry 2002, 277(36):32837-32842.
29. Goder V., Spiess M. Topogenesis of membrane proteins: Determinants and dynamics. FEBS Letters 2001, 504(3):87-93.
30. Grefhorst A., Schreurs M., Oosterveer M.H., Cortés V.A., Havinga R., Herling A.W., et al. Carbohydrate-response-element-binding protein (ChREBP) and not the liver X receptor α (LXRα) mediates elevated hepatic lipogenic gene expression in a mouse model of glycogen storage disease type 1. Biochemical Journal 2010, 432(2):249-254.
31. Hall J.A., Fann M.C., Maloney P.C. Altered substrate selectivity in a mutant of an intrahelical salt bridge in UhpT, the sugar phosphate carrier of Escherichia coli. Journal of Biological Chemistry 1999, 274(10):6148-6153.
32. He L., Vasiliou K., Nebert D.W. Analysis and update of the human solute carrier (SLC) gene superfamily. Human Genomics 2009, 3(2):195-206.
33. Hemmerle H., Burger H.J., Below P., Schubert G., Rippel R., Schindler P.W., et al. Chlorogenic acid and synthetic chlorogenic acid derivatives: Novel inhibitors of hepatic glucose-6-phosphate translocase. Journal of Medicinal Chemistry 1997, 40(2):137-145.
34. Herling A.W., Burger H., Schubert G., Hemmerle H., Schaefer H., Kramer W. Alterations of carbohydrate and lipid intermediary metabolism during inhibition of glucose-6-phosphatase in rats. European Journal of Pharmacology 1999, 386(1):75-82.
35. Hiraiwa H., Pan C.-J., Lin B., Moses S.W., Chou J.Y. Inactivation of the glucose-6-phosphate transporter causes glycogen storage disease type 1b. Journal of Biological Chemistry 1999, 274(9):5532-5536.
36. Hoffman K., Stoffel W. TMbase-A database of membrane spanning protein segments. Biological Chemistry Hoppe-Seyler 1993, 347:166-170.
37. Huang Y., Lemieux M.J., Song J., Auer M., Wang D.N. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 2003, 301(5633):616-620.
38. Iacopetta D., Lappano R., Cappello A.R., Madeo M., De Francesco E.M., Santoro A., et al. SLC37A1 gene expression is up-regulated by epidermal growth factor in breast cancer cells. Breast Cancer Research and Treatment 2010, 122(3):755-764.
39. Jackson M.R., Nilsson T., Peterson P.A. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO Journal 1990, 9(10):3153-3162.
40. Jackson M.R., Nilsson T., Peterson P.A. Retrieval of transmembrane proteins to the endoplasmic reticulum. Journal of Cell Biology 1993, 121(2):317-333.
41. Janecke A.R., Linder M., Erdel M., Mayatepek E., Moslinger D., Podskarbi T., et al. Mutation analysis in glycogen storage disease type 1 non-a. Human Genetics 2000, 107(3):285-289.
42. Jun H.S., Cheung Y.Y., Lee Y.M., Mansfield B.C., Chou J.Y. Glucose-6-phosphatase-β, implicated in a congenital neutropenia syndrome, is essential for macrophage energy homeostasis and functionality. Blood 2012, 119(17):4047-4055.
43. Jun H.S., Lee Y.M., McDermott D.H., DeRavin S.S., Murphy P.M., Mansfield B.C., et al. Lack of glucose recycling between endoplasmic reticulum and cytoplasm underlies cellular dysfunction in glucose-6-phosphatase-beta-deficient neutrophils in a congenital neutropenia syndrome. Blood 2010, 116(15):2783-2792.
44. Kim J.Y., Tillison K., Zhou S., Wu Y., Smas C.M. The major facilitator superfamily member Slc37a2 is a novel macrophage- specific gene selectively expressed in obese white adipose tissue. American Journal of Physiology. Endocrinology and Metabolism 2007, 293(1):E110-E120.
45. Landolt-Marticorena C., Reithmeier R.A.F. Asparagine-linked oligosaccharides are localized to single extracytosolic segments in multi-span membrane glycoproteins. Biochemical Journal 1994, 302(Pt 1):253-260.
46. Lei K.-J., Chen H., Pan C.-J., Ward J.M., Mosinger B., Lee E.J., et al. Glucose-6-phosphatase dependent substrate transport in the glycogen storage disease type 1a mouse. Nature Genetics 1996, 13(2):203-209.
47. Lei K.-J., Shelly L.L., Pan C.-J., Sidbury J.B., Chou J.Y. Mutations in the glucose-6-phosphatase gene that cause glycogen storage disease type 1a. Science 1993, 262(5133):580-583.
48. Leuzzi R., Fulceri R., Marcolongo P., Bánhegyi G., Zammarchi E., Stafford K., et al. Glucose 6-phosphate transport in fibroblast microsomes from glycogen storage disease type 1b patients: Evidence for multiple glucose 6-phosphate transport systems. Biochemical Journal 2001, 357(Pt 2):557-562.
49. Lin B., Annabi B., Hiraiwa H., Pan C.-J., Chou J.Y. Cloning and characterization of cDNAs encoding a candidate glycogen storage disease type 1b protein in rodents. Journal of Biological Chemistry 1998, 273(48):31656-31670.
50. Lin B., Pan C.-J., Chou J.Y. Human variant glucose-6-phosphate transporter is active in microsomal transport. Human Genetics 2000, 107(5):526-529.
51. Lloyd A.D., Kadner R.J. Topology of the Escherichia coli UhpT sugar-phosphate transporter analyzed by using TnphoA fusions. Journal of Bacteriology 1990, 172(4):1688-1693.
52. Molinari M. N-glycan structure dictates extension of protein folding or onset of disposal. Nature Chemical Biology 2007, 3(6):313-320.
53. Nilsson I.M., von Heijne G. Determination of the distance between the oligosaccharyltransferase active site and the endoplasmic reticulum membrane. Journal of Biological Chemistry 1993, 268(8):5798-5801.
54. Nordlie R.C., Sukalski K.A., Munoz J.M., Baldwin J.J. Type 1c, a novel glycogenosis. Journal of Biological Chemistry 1983, 258:9739-9744.
55. Pan C.J., Chen S.Y., Jun H.S., Lin S.R., Mansfield B.C., Chou J.Y. SLC37A1 and SLC37A2 are phosphate-linked, glucose-6-phosphate antiporters. PLoS One 2011, 6(9):e23157.
56. Pan C.J., Chen S.Y., Lee S., Chou J.Y. Structure-function study of glucose-6-phosphate transporter, an eukaryotic antiporter deficient in glycogen storage disease type Ib. Molecular Genetics and Metabolism 2009, 96(1):32-37.
57. Pan C.J., Chen L.Y., Mansfield B.C., Salani B., Varesio L., Chou J.Y. The signature motif in human glucose-6-phosphate transporter is essential for microsomal transport of glucose-6-phosphate. Human Genetics 2003, 112(4):430-433.
58. Pan C.-J., Lin B., Chou J.Y. Transmembrane topology of human glucose-6-phosphate transporter. Journal of Biological Chemistry 1999, 274(20):13865-13869.
59. Pao S.S., Paulsen I.T., Saier M.H. Major facilitator superfamily. Microbiology and Molecular Biology Reviews 1998, 62(1):1-34.
60. Parodi A.J. Protein glucosylation and its role in protein folding. Annual Review of Biochemistry 2000, 69:69-93.
61. Qiu Z.Q., Lu C.X., Wang W., Qiu J.J., Wei M. Mutation in the SLC37A4 gene of glycogen storage disease type Ib in 15 families of the mainland of China. Zhonghua Er Ke Za Zhi. Chinese Journal of Pediatrics 2011, 49(3):203-208.
62. Reddy V.S., Shlykov M.A., Castillo R., Sun E.I., Saier M.H. The major facilitator superfamily (MFS) revisited. FEBS Journal 2012, 279(11):2022-2035.
63. Shieh J.-J., Pan C.-J., Mansfield B.C., Chou J.Y. Glucose-6-phosphate hydrolase, widely expressed outside the liver, can explain age-dependent resolution of hypoglycemia in glycogen storage disease type Ia. Journal of Biological Chemistry 2003, 278(47):47098-47103.
64. Takahashi Y., Miyata M., Zheng P., Imazato T., Horwitz A., Smith J.D. Identification of cAMP analogue inducible genes in RAW264 macrophages. Biochimica et Biophysica Acta 2000, 1492(2-3):385-394.
65. Veiga-da-Cunha M., Gerin I., Chen Y.-T., de Barsy T., de Lonlay P., Dionisi-Vici C., et al. A gene on chromosome 11q23 coding for a putative glucose-6-phosphate translocase is mutated in glycogen-storage disease types Ib and Ic. American Journal of Human Genetics 1998, 63(4):976-983.
66. Veiga-da-Cunha M., Gerin I., Chen Y.-T., Lee P.J., Leonard J.V., Maire I., et al. The putative glucose 6-phosphate translocase gene is mutated in essentially all cases of glycogen storage disease type I non-a. European Journal of Human Genetics 1999, 7(16):717-723.
67. Zingone A., Hiraiwa H., Pan C.-J., Lin B., Chen H., Ward J.M., et al. Correction of glycogen storage disease type 1a in a mouse model by gene therapy. Journal of Biological Chemistry 2000, 275(2):828-832.