Calreticulin is essential for cardiac development

Journal of Cell Biology

Volumn 144, Issue 5, 1999, Pages 857-868

  Mesaeli, Nasrin ^a   Nakamura, Kimitoshi ^a   Zvaritch, Elena ^b   Dickie, Peter ^a   Dziak, Ewa ^b   Krause, Karl Heinz ^c   Opas, Michal ^b   MacLennan, David H ^b   Michalak, Marek ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Calcineurin; Calcium binding protein; Cardiac development; Endoplasmic reticulum; NF AT; Transcription

Indexed keywords

CALCIUM BINDING PROTEIN; CALRETICULIN; NUCLEAR FACTOR;

ARTICLE; CALCIUM HOMEOSTASIS; ENDOPLASMIC RETICULUM; GENE ACTIVATION; GENE TARGETING; HEART DEVELOPMENT; HEART VENTRICLE HYPERTROPHY; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; REPORTER GENE;

ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM-BINDING PROTEINS; CALRETICULIN; CELL NUCLEUS; DNA PRIMERS; DNA-BINDING PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; HEART; INOSITOL 1,4,5-TRISPHOSPHATE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHENOTYPE; PROMOTER REGIONS (GENETICS); RIBONUCLEOPROTEINS; TRANSCRIPTION FACTORS;

MUS MUSCULUS;

EID: 0033535353     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.5.857     Document Type: Article

References (64)

1. 2+ binding protein calreticulin and perform, a component of the T-cell granules. Biochemistry. 37:10386-10394.
2. Ausuhel, F.M., R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhe. 1989. Current Protocols in Molecular Biology. Vol. 1-3. John Wiley & Sons. Inc., New York.
3. 2+ binding domains. J. Biol. Chem. 266:21458-21-165.
4. 2+ stores and reveals aspects of their lumenal microenvironment and function. J. Cell Biol. 130:847-855.
5. Brillantes, A.B., K. Ondrias, A. Scott, E. Kobrinsky, E. Ondriasova, M.C. Moschella, T. Jayaraman, M. Lander, B.E. Ehrlich, and A.R. Marks. 1994. Stabilisation of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell. 77:513-523.
6. Burns, K., C.D. Helgason, R.C. Bleackley, and M. Michalak. 1992. Calreticulin in T-lymphocytes. Identification of calreticulin in T-lymphocytes and demonstration that activation of T-cells correlates with increased levels of calreticulin mRNA and protein. J. Biol. Chem. 267:19039-19042.
7. Burns, K., B. Duggan, A.E. Atkinson, K.S. Famulski, M. Nemer, R.C. Bleackley, and M. Michalak. 1994. Modulation of gene expression by calreticulin binding to the glucocorticoid receptor. Nature. 367:476-480.
8. Byrne, W.J. 1991. Disorders of the umbilical cord, abdominal wall, urachus, and omphalomesenteric duct. In Diseases of the Newborn. H.W. Tacusch, R.A. Ballard, and M.E. A very, editors. W.B. Saunders Co. Philadelphia. 694-701.
9. 2+ waves. Cell. 82:765-771.
10. Cameron, A.M., J.P. Steiner, D.M. Sabatini, A.I. Kaplin, L.D. Walensky, and S.U. Snyder. 1995. Immunophilin FK506 binding protein associated with inositol 1,4.5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. USA. 92:1784-1788.
11. Chen, J., S. Chang, S.A. Duncan, H.J. Okano, G. Fishell, and A. Aderem. 1996. Disruption of the MARCKS gene prevents cranial neural tube closure and results in anencephaly. Proc. Natl. Acad. Sci. USA. 93:6275-6279.
12. 1 with calreticulin. J. Biol. Chem. 270:23132-23138.
13. Coppolino, M., M.J. Woodside, N. Demaurex, S. Grinstein, R. St-Arnaud, and S. Dedhar. 1997. Calreticulin is essential for integrin-mediated calcium signaling and cell adhesion. Nature. 386:843-847.
14. Creazzo, T.L., R.F. Godt, L. Leatherbury, S.J. Conway, and M.L. Kirby. 1998. Role of cardiac neural crest cells in cardiovascular development. Annu. Rev. Physiol. 60:267-286.
15. de la Pompa, J.L., L.A. Timmerman, H. Takimoto, H. Yoshida, A.J. Elia, E. Saniper, J. Potter, L. Marengere, B.L. Langille, G.R. Crabtree, et al. 1998. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature. 392:182-185.
16. Dedhar, S., P.S. Rennie, M. Shago, C.Y. Hagesteijn, H. Yang, J. Filmus, R.G. Hawley, N. Bruchovsky, H. Cheng, R.J. Matusik, et al. 1994. Inhibition of nuclear hormone receptor activity by calreticulin. Nature. 367:480-483.
17. DeRuiter, M.C., R.E. Poelmann, I. VanderPlas-de Vries, M.M. Mentink, and A.C. Gittenberger-de Groot. 1992. The development of the myocardium and endocardium in mouse embryos. Fusion of two heart tubes? Anat. Embryol. 185:461-473.
18. 2+ response amplitude and duration. Nature. 386:855-858.
19. Dupuis, M., E. Schaerer, K.-H. Krause, and J. Tschopp. 1993. The calcium binding protein calreticulin is a major constituent of lytic granules in cytolytic T lymphocytes. J. Exp. Med. 177:1-7.
20. Eggenschwiler, J., T. Ludwig, P. Fisher, P.A. Leighton, S.M. Tilghman, and A. Efstratiadis. 1997. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes, Genes Dev. 11:3128-3342.
21. Evans, T. 1997. Regulation of cardiac gene expression by GATA-4/5/6. Trends Card. Med. 7:75-83.
22. Fasolato, C., P. Pizzo, and T. Prozzan. 1998. Delayed activation of the storeoperated calcium current induced by calreticulin overexpression in RBL-1 cells. Mol. Biol. Cell. 9:1513-1522.
23. Fishman, M.C., and K.R. Chien. 1997. Fashioning the vertebrate heart: earliest embryonic decisions. Development. 124:2099-2117.
24. Fliegel, L., K. Burns, D.H. MacLennan, R.A.F. Reithmeier, and M. Michalak. 1989a. Molecular cloning of the high affinity calcium binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 264: 21522-21528.
25. Fliegel, L., K. Burns, M. Opas, and M. Michalak. 1989b. The high affinity calcium binding protein of skeletal muscle sarcoplasmic reticulum. Biochim. Biophys. Acta. 982:1-8.
26. Gao, X., T. Sedgwick, Y.-B. Shi, and T. Evans. 1998. Distinct functions are implicated for the GATA-4, -5, and -6 transcription factors in the regulation of intestine epithelial cell differentiation. Mol. Cell Biol. 18:2901-2911.
27. Grepin, C., L. Dagnino, L. Robitaille, L. Haberstroh, T. Antakly, and M. Nemer. 1994. A hormone-encoding gene identifies a pathway for cardiac but not skeletal muscle gene transcription. Mol. Cell Biol. 14:3115-3129.
28. 2+ influx in voltage-clamped ras-transformed NTH/3T3 fibroblasts. J. Biol. Chem. 268: 19403-19410.
29. Helenius, A., E.S. Trombetta, D.N. Hebert, and J.F. Simons. 1997. Calnexin, calreticulin and the folding of glycoproteins. Trends. Cell Biol. 7:193-200.
30. John, L.M., J.D. Lechleiter, and P. Camacho. 1998. Differential modulation of SERCA2 isoforms by calreticulin. J. Cell Biol. 142:963-973.
31. Kaufman, M.H. 1992. The atlas of mouse development. Academic Press, London.
32. Kehlenbach, R.H., A. Dickmanns, and L. Gerace. 1998. Nucleocytoplasmic shuttling factor including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141:863-874.
33. Krause, K.-H., and M. Michalak. 1997. Calreticulin. Cell. 88:439-443.
34. Kuo, C.T., E.E. Morrisey, R. Anandappa, K. Sigrist, M.M. Lu, M.S. Parmacek, C. Soudais, and J.M. Leiden. 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Der. 11:8145-8149.
35. 4. Nature. 227:680-685.
36. 2+ response to brady kinin and increases sensitivity to ionomycin in NG-108-15 cells. J. Biol. Chem. 269:28635-28639.
37. 2+ influx. J. Biol. Chem. 271:9332-9339.
38. Michalak, M., R.E. Milner, K. Burns, and M. Opas. 1992. Calreticulin. Biochem. J. 285:681-692.
39. Michalak, M., K. Burns, C. Andrin, N. Mesaeli, G.H. Jass, J.L. Busaan, and M. Opas. 1996. Endoplasmic reticulum form of calreticulin modulates glucocorticoid-sensitive gene expression. J. Biol. Chem. 271:29436-29445.
40. Mikawa, T., and D.A. Fischman. 1996. The polyclonal origin of myocyte lineages. Annu. Rev. Physiol. 58:509-521.
41. Milner, R.E., S. Baksh, C. Shemanko, J.E. Vance, M. Carpenter, L. Smillie, M. Opas, and M. Michalak. 1991. Calreticulin, and not calsequestrin, is the major calcium binding protein of smooth muscle sarcoplasmic reticulum and liver endoplasmic reticulum. J. Biol. Chem. 266:7155-7156.
42. Molkentin, J.D., Q. Lin, S.A. Duncan, and E.N. Olson. 1997. Requirement of the transcription factor GATA-4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061-1072.
43. Molkentin, J.D., J.R. Lu, C.L. Antos, B. Markham, J. Richardson, J. Robbins, S.R. Grant, and E.N. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:215-228.
44. Nakamura, M., M. Moriya, T. Baba, Y. Michikawa, T. Yamanobe, K. Arai, S. Okinaga, and T. Kobayashi. 1993. An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp. Cell Res. 205: 101-110.
45. Nauseef, W.M., S.J. McCormick, and R.A. Clark. 1995. Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J. Biol. Chem. 270:4741-4747.
46. 2+-binding proteins and numbers of the thioredoxin superfamily. J. Biol. Chem. 269:1744-1749.
47. Olson, E.N., and D. Srivastova. 1996. Molecular pathways controlling heart development. Science. 272:617-676.
48. Opas, M., M. Szewczenko-Pawlikowski, G.K. Jass, N. Mesaeli, and M. Michalak. 1996. Calreticulin modulates cell adhesiveness via regulation of vinculin expression. J. Cell Biol. 135:1913-1923.
49. Ostwald, T.J., and D.H. MacLennan. 1974. Isolation of a high affinity calcium binding protein from sarcoplasmic reticulum. J. Biol. Chem. 249:974-979.
50. Ranger, A.M., M.J. Grusby, M.R. Hodge, E.M. Gravallese, F.C. de la Brousse, T. Hoey, C. Mickanin, H.S. Baldwin, and L.H. Glimcher. 1998. The transcription factor NF-ATc is essential for cardiac valve formation. Nature. 392: 186-190.
51. Rao, A., C. Luo, and P.G. Hogan. 1997. Transcription factors of the NF-AT family: regulation and function. Annu. Rev. Immunol. 15:707-747.
52. Rossant, J. 1996. Mouse mutants and cardiac development. Circ. Res. 78:349-353.
53. Shou, W., B. Aghdasi, D.L. Armstrong, Q. Guo, S. Bao, M.J. Charng, L.M. Mathews, M.D. Schneider, S.L. Hamilton, and M.M. Matzuk. 1998. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature. 391:489-492.
54. Singh, N.K., C.D. Atreya, and H.L. Nakhasi. 1994. Identification of calreticulin as a rubella virus RNA binding protein. Proc. Natl. Acad. Sci. USA, 91: 12770-12774.
55. Sontheimer, R.D., T.-S. Lieu, and J.D. Capra. 1993. Calreticulin: the diverse functional repertoire of a new human autoantigen. Immunologist. 1:155-160.
56. 2+ stores during phagocytosis in human neutrophils. Science. 265:1439-1441.
57. Stumpo, D.J., C.B. Bock, J.S. Tuttle, and P.J. Blackshear. 1995. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc. Natl. Acad. Sci. USA. 92:944-948.
58. Sucov, H.M. 1998. Molecular insights into cardiac development. Annu. Rev. Physiol. 60:287-308.
59. Taketo, M., A.C. Schroeder, L.E. Mobraaten, K.B. Gunning, G. Hanten, R.R. Fox, T.H. Roderick, C.L. Stewart, F. Lilly, C.T. Hansen, et al. 1991. FVB/N: an inbred mouse strain preferable for transgenic analyses. Proc. Natl. Acad. Sci. USA. 88:2065-2069.
60. Tharin, S., P.A. Hamel, E.M. Conway, M. Michalak, and M. Opas. 1996. Regulation of calcium storage proteins, calreticulin and calsequestrin, during differentiation of the myogenic cell line L6. J. Cell Physiol. 166:547-560.
61. 2+-ATPasc. Proc. Natl. Acad. Sci. USA. 87:2466-2470.
62. 2+ signals and immunosuppression. Nature. 383:837-840.
63. Waser, M., N. Mesaeli, C. Spencer, and M. Michalak. 1997. Regulation of calreticulin gene expression by calcium. J. Cell Biol. 138:547-557.
64. KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature. 387:151-158.