TAT-mediated transduction of MafA protein in Utero results in enhanced pancreatic insulin expression and changes in islet morphology

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Vargas, Nancy ^a   Álvarez Cubela, Silvia ^a   Giraldo, Jaime A ^a,b   Nieto, Margarita ^a   Fort, Nicholas M ^a   Cechin, Sirlene ^a   García, Enrique ^a   Espino Grosso, Pedro ^a   Fraker, Christopher A ^a,b   Ricordi, Camillo ^a   Inverardi, Luca ^a   Pastori, Ricardo L ^a   Domínguez Bendala, Juan ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Miami College of Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; NEUROGENIN 3; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR PDX 1; HYBRID PROTEIN; MAFA PROTEIN, MOUSE; TRANSCRIPTION FACTOR MAF;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EMBRYO; FEMALE; GENETIC REGULATION; IN VITRO STUDY; MOUSE; NONHUMAN; PANCREAS ISLET CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; NEWBORN; PANCREAS; PANCREAS ISLET; PREGNANCY; PRENATAL DEVELOPMENT; PROMOTER REGION; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; UTERUS; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; GENE EXPRESSION; GENE PRODUCTS, TAT; INSULIN; ISLETS OF LANGERHANS; MAF TRANSCRIPTION FACTORS, LARGE; MALE; MICE; MICE, INBRED C57BL; PANCREAS; PREGNANCY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; UTERUS;

EID: 79961159102     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022364     Document Type: Article

References (50)

1. Nishizawa M, Kataoka K, Goto N, Fujiwara KT, Kawai S, (1989) v-maf, a viral oncogene that encodes a "leucine zipper" motif. Proc Natl Acad Sci U S A 86: 7711-7715.
2. Ogino H, Yasuda K, (1998) Induction of lens differentiation by activation of a bZIP transcription factor, L-Maf. Science 280: 115-118.
3. Blank V, Andrews NC, (1997) The Maf transcription factors: regulators of differentiation. Trends Biochem Sci 22: 437-441.
4. Nishimura W, Kondo T, Salameh T, El Khattabi I, Dodge R, et al. (2006) A switch from MafB to MafA expression accompanies differentiation to pancreatic beta-cells. Dev Biol 293: 526-539.
5. Zhang C, Moriguchi T, Kajihara M, Esaki R, Harada A, et al. (2005) MafA is a key regulator of glucose-stimulated insulin secretion. Mol Cell Biol 25: 4969-4976.
6. Nishimura W, Rowan S, Salameh T, Maas RL, Bonner-Weir S, et al. (2008) Preferential reduction of beta cells derived from Pax6-MafB pathway in MafB deficient mice. Dev Biol 314: 443-456.
7. Artner I, Blanchi B, Raum JC, Guo M, Kaneko T, et al. (2007) MafB is required for islet beta cell maturation. Proc Natl Acad Sci U S A 104: 3853-3858.
8. Matsuoka TA, Zhao L, Artner I, Jarrett HW, Friedman D, et al. (2003) Members of the large Maf transcription family regulate insulin gene transcription in islet beta cells. Mol Cell Biol 23: 6049-6062.
9. Shieh SY, Tsai MJ, (1991) Cell-specific and ubiquitous factors are responsible for the enhancer activity of the rat insulin II gene. J Biol Chem 266: 16708-16714.
10. Zhao L, Guo M, Matsuoka TA, Hagman DK, Parazzoli SD, et al. (2005) The islet beta cell-enriched MafA activator is a key regulator of insulin gene transcription. J Biol Chem 280: 11887-11894.
11. Aramata S, Han SI, Kataoka K, (2007) Roles and regulation of transcription factor MafA in islet beta-cells. Endocr J 54: 659-666.
12. Deutsch G, Jung J, Zheng M, Lora J, Zaret KS, (2001) A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 128: 871-881.
13. Kaneto H, Matsuoka TA, Nakatani Y, Miyatsuka T, Matsuhisa M, et al. (2005) A crucial role of MafA as a novel therapeutic target for diabetes. J Biol Chem 280: 15047-15052.
14. Huang HP, Liu M, El-Hodiri HM, Chu K, Jamrich M, et al. (2000) Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3. Mol Cell Biol 20: 3292-3307.
15. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA, (2008) In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455: 627-632.
16. Wang H, Brun T, Kataoka K, Sharma AJ, Wollheim CB, (2007) MAFA controls genes implicated in insulin biosynthesis and secretion. Diabetologia 50: 348-358.
17. Kaneto H, Miyatsuka T, Fujitani Y, Noguchi H, Song KH, et al. (2007) Role of PDX-1 and MafA as a potential therapeutic target for diabetes. Diabetes Res Clin Pract 77 (Suppl 1): S127-137.
18. Chiou SH, Chen SJ, Chang YL, Chen YC, Li HY, et al. (2011) MafA promotes the reprogramming of placenta-derived multipotent stem cells into pancreatic islets-like and insulin-positive cells. J Cell Mol Med.
19. Harui A, Suzuki S, Kochanek S, Mitani K, (1999) Frequency and stability of chromosomal integration of adenovirus vectors. J Virol 73: 6141-6146.
20. Baum C, Kustikova O, Modlich U, Li Z, Fehse B, (2006) Mutagenesis and oncogenesis by chromosomal insertion of gene transfer vectors. Hum Gene Ther 17: 253-263.
21. Wadia JS, Dowdy SF, (2003) Modulation of cellular function by TAT mediated transduction of full length proteins. Curr Protein Pept Sci 4: 97-104.
22. Tyagi M, Rusnati M, Presta M, Giacca M, (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276: 3254-3261.
23. Kaplan IM, Wadia JS, Dowdy SF, (2005) Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 102: 247-253.
24. Zaro JL, Shen WC, (2003) Quantitative comparison of membrane transduction and endocytosis of oligopeptides. Biochem Biophys Res Commun 307: 241-247.
25. Embury J, Klein D, Pileggi A, Ribeiro M, Jayaraman S, et al. (2001) Proteins linked to a protein transduction domain efficiently transduce pancreatic islets. Diabetes 50: 1706-1713.
26. Fornoni A, Pileggi A, Molano RD, Sanabria NY, Tejada T, et al. (2008) Inhibition of c-jun N terminal kinase (JNK) improves functional beta cell mass in human islets and leads to AKT and glycogen synthase kinase-3 (GSK-3) phosphorylation. Diabetologia 51: 298-308.
27. Klein D, Mendoza V, Pileggi A, Molano RD, Barbe-Tuana FM, et al. (2005) Delivery of TAT/PTD-fused proteins/peptides to islets via pancreatic duct. Cell Transplant 14: 241-248.
28. Klein D, Ribeiro MM, Mendoza V, Jayaraman S, Kenyon NS, et al. (2004) Delivery of Bcl-XL or its BH4 domain by protein transduction inhibits apoptosis in human islets. Biochem Biophys Res Commun 323: 473-478.
29. Mendoza V, Klein D, Ichii H, Ribeiro MM, Ricordi C, et al. (2005) Protection of islets in culture by delivery of oxygen binding neuroglobin via protein transduction. Transplant Proc 37: 237-240.
30. Ribeiro MM, Klein D, Pileggi A, Molano RD, Fraker C, et al. (2003) Heme oxygenase-1 fused to a TAT peptide transduces and protects pancreatic beta-cells. Biochem Biophys Res Commun 305: 876-881.
31. Rehman KK, Bertera S, Bottino R, Balamurugan AN, Mai JC, et al. (2003) Protection of islets by in situ peptide-mediated transduction of the Ikappa B kinase inhibitor Nemo-binding domain peptide. J Biol Chem 278: 9862-9868.
32. Pastori RL, Klein D, Ribeiro MM, Ricordi C, (2004) Delivery of proteins and peptides into live cells by means of protein transduction domains: potential application to organ and cell transplantation. Transplantation 77: 1627-1631.
33. Domínguez-Bendala CRaRP J, (2006) Protein transduction: a novel approach to induce in vitro pancreatic differentiation. Cell Transplantation 15: 85-90.
34. Domínguez-Bendala J, Klein D, Ribeiro M, Ricordi C, Inverardi L, et al. (2005) TAT-mediated neurogenin 3 protein transduction stimulates pancreatic endocrine differentiation in vitro. Diabetes 54: 720-726.
35. Hay CW, Docherty K, (2006) Comparative analysis of insulin gene promoters: implications for diabetes research. Diabetes 55: 3201-3213.
36. Guo S, Burnette R, Zhao L, Vanderford NL, Poitout V, et al. (2009) The stability and transactivation potential of the mammalian MafA transcription factor are regulated by serine 65 phosphorylation. J Biol Chem 284: 759-765.
37. Guo S, Vanderford NL, Stein R, (2010) Phosphorylation within the MafA N terminus regulates C-terminal dimerization and DNA binding. J Biol Chem 285: 12655-12661.
38. Nishimura W, Bonner-Weir S, Sharma A, (2009) Expression of MafA in pancreatic progenitors is detrimental for pancreatic development. Dev Biol 333: 108-120.
39. Carvalho CP, Martins JC, da Cunha DA, Boschero AC, Collares-Buzato CB, (2006) Histomorphology and ultrastructure of pancreatic islet tissue during in vivo maturation of rat pancreas. Ann Anat 188: 221-234.
40. Collares-Buzato CB, Carvalho CP, Furtado AG, Boschero AC, (2004) Upregulation of the expression of tight and adherens junction-associated proteins during maturation of neonatal pancreatic islets in vitro. J Mol Histol 35: 811-822.
41. Carvalho CP, Barbosa HC, Britan A, Santos-Silva JC, Boschero AC, et al. (2010) Beta cell coupling and connexin expression change during the functional maturation of rat pancreatic islets. Diabetologia 53: 1428-1437.
42. Kwon YD, Oh SK, Kim HS, Ku SY, Kim SH, et al. (2005) Cellular manipulation of human embryonic stem cells by TAT-PDX1 protein transduction. Mol Ther 12: 28-32.
43. Liu A, Joyner AL, Turnbull DH, (1998) Alteration of limb and brain patterning in early mouse embryos by ultrasound-guided injection of Shh-expressing cells. Mech Dev 75: 107-115.
44. Punzo C, Cepko CL, (2008) Ultrasound-guided in utero injections allow studies of the development and function of the eye. Dev Dyn 237: 1034-1042.
45. Strasburger JF, Wakai RT, (2010) Fetal cardiac arrhythmia detection and in utero therapy. Nat Rev Cardiol 7: 277-290.
46. Lajic S, Nordenstrom A, Hirvikoski T, (2008) Long-term outcome of prenatal treatment of congenital adrenal hyperplasia. Endocr Dev 13: 82-98.
47. Yinon YM, Visser JM, Kelly ENM, Windrim RM, Amsalem HM, et al. (2010) Early intra-uterine transfusions in severe red blood cell alloimmunization. Ultrasound Obstet Gynecol.
48. Galligan BR, Cairns R, Schifano JV, Selbing A, Bernvil SS, (1989) Preparation of packed red cells suitable for intravascular transfusion in utero. Transfusion 29: 179-181.
49. Benkhelifa S, Provot S, Nabais E, Eychene A, Calothy G, et al. (2001) Phosphorylation of MafA is essential for its transcriptional and biological properties. Mol Cell Biol 21: 4441-4452.
50. Sambrook J, Russell D, (2001) Molecular Cloning: a laboratory manual Cold Spring Harbor, New York Cold Spring Harbor Laboratory Press.