CoChat
Sign Up
Cited by 139Congenital heart defects researchCardiomyopathy and Myosin StudiesCardiac electrophysiology and arrhythmias

Targeted Disruption of the Murine Bin1/Amphiphysin II Gene Does Not Disable Endocytosis but Results in Embryonic Cardiomyopathy with Aberrant Myofibril Formation

Open access
Muller, Alexander J., Baker, Judith F., DuHadaway, James B., Ge, Kai, Farmer, George, Donover, P. Scott, Meade, Raymond, Reid, Christian +5 more·2003·Molecular and Cellular Biology
DOI 10.1128/mcb.23.12.4295-4306.2003PMC PMC156129
Open this paper in CoChat — free account

Abstract

The mammalian Bin1/Amphiphysin II gene encodes an assortment of alternatively spliced adapter proteins that exhibit markedly divergent expression and subcellular localization profiles. Bin1 proteins have been implicated in a variety of different cellular processes, including endocytosis, actin cytoskeletal organization, transcription, and stress responses. To gain insight into the physiological functions of the Bin1 gene, we have disrupted it by homologous recombination in the mouse. Bin1 loss had no discernible impact on either endocytosis or phagocytosis in mouse embryo-derived fibroblasts and macrophages, respectively. Similarly, actin cytoskeletal organization, proliferation, and apoptosis in embryo fibroblasts were all unaffected by Bin1 loss. In vivo, however, Bin1 loss resulted in perinatal lethality. Bin1 has been reported to affect muscle cell differentiation and T-tubule formation. No striking histological abnormalities were evident in skeletal muscle of Bin1 null embryos, but severe ventricular cardiomyopathy was observed in these embryos. Ultrastructurally, myofibrils in ventricular cardiomyocytes of Bin1 null embryos were severely disorganized. These results define a developmentally critical role for the Bin1 gene in cardiac muscle development.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/mcb.23.12.4295-4306.2003

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Neuronal cultures from Bin1−/− mice failed to reveal a deficiency in basal synaptic vesicle uptake.

    “However, neuronal cultures prepared from Bin1−/− mice failed to reveal a deficiency in basal synaptic vesicle uptake [10], raising the possibility that BIN1 and Amphiphysin 1 may have divergent functions in the brain.”

    From Predominant expression of Alzheimer’s disease-associated BIN1 in mature oligodendrocytes and localization to white matter tracts (2016) · cites this paper as [10]

    The Results report that cultured Bin1−/− cortical neurons showed no excess clathrin-coated vesicles at synapses, supporting the absence of an apparent vesicle-processing defect. But the Discussion says direct evaluation in cultured neurons is still necessary to assess synaptic vesicle endocytosis. Its statement about unchanged basal uptake concerns AmphI knockout mice with reduced neuronal Bin1 isoforms, not Bin1−/− neuronal cultures. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • The specificities of the two BIN1 mAbs (2F11 and 99D) have been well established and confirmed by transfection studies in HEK293 cells using BIN1 isoform 7.

    “The specificities of the two BIN1 mAbs have been well established [10, 13, 47] and confirmed by transfection studies in HEK293 cells using BIN1 isoform 7 [which lacks the exon 7-encoded sequences] (Additional file 6: Figure 2SC).”

    From Predominant expression of Alzheimer’s disease-associated BIN1 in mature oligodendrocytes and localization to white matter tracts (2016) · cites this paper as [10]

  • Loss of BIN1 function neither impaired endocytic transferrin uptake in Bin1−/− fibroblasts nor phagocytic internalization of zymosan.

    “the loss of BIN1 function neither impaired endocytic transferrin uptake in Bin1−/− fibroblasts nor phagocytic internalization of zymosan [10].”

    From Predominant expression of Alzheimer’s disease-associated BIN1 in mature oligodendrocytes and localization to white matter tracts (2016) · cites this paper as [10]

  • Cellular transferrin levels were increased in Bin1 KO MEFs without an effect on transferrin internalization.

    “Consistent with this, cellular transferrin levels were increased in Bin1 KO MEFs without an effect on transferrin internalization (18).”

    From BIN1 regulates BACE1 intracellular trafficking and amyloid-β production (2016) · cites this paper as [18]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 63

  1. [1]Balguerie, A., P. Sivadon, M. Bonneu, and M. Aigle. 1999. Rvs167p, the budding yeast homolog of amphiphysin, colocalizes with actin patches. J. Cell Sci. 112(Pt. 15):2529-2537. [DOI] [PubMed] [Google Scholar]
  2. [2]Banker, G. A., and K. Goslin. 1991. Culturing nerve cells. MIT Press, Cambridge, Mass.
  3. [3]Bauer, F., M. Urdaci, M. Aigle, and M. Crouzet. 1993. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol. Cell. Biol. 13:5070-5084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. [4]Bonne, G., L. Carrier, P. Richard, B. Hainque, and K. Schwartz. 1998. Familial hypertrophic cardiomyopathy: from mutations to functional defects. Circ. Res. 83:580-593. [DOI] [PubMed] [Google Scholar]
  5. [5]Breton, A. M., and M. Aigle. 1998. Genetic and functional relationship between Rvsp, myosin and actin in Saccharomyces cerevisiae. Curr. Genet. 34:280-286. [DOI] [PubMed] [Google Scholar]
  6. [6]Brizzio, V., A. E. Gammie, and M. D. Rose. 1998. Rvs161p interacts with Fus2p to promote cell fusion in Saccharomyces cerevisiae. J. Cell Biol. 141:567-584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. [8]Colwill, K., D. Field, L. Moore, J. Friesen, and B. Andrews. 1999. In vivo analysis of the domains of yeast Rvs167p suggests Rvs167p function is mediated through multiple protein interactions. Genetics 152:881-893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. [9]Cremona, O., G. Di Paolo, M. R. Wenk, A. Luthi, W. T. Kim, K. Takei, L. Daniell, Y. Nemoto, S. B. Shears, R. A. Flavell, D. A. McCormick, and P. De Camilli. 1999. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179-188. [DOI] [PubMed] [Google Scholar]
  9. [10]Crouzet, M., M. Urdaci, L. Dulau, and M. Aigle. 1991. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene. Yeast 7:727-743. [DOI] [PubMed] [Google Scholar]
  10. [11]David, C., P. S. McPherson, O. Mundigl, and P. de Camilli. 1996. A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA 93:331-335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. [12]Di Paolo, G., S. Sankaranarayanan, M. R. Wenk, L. Daniell, E. Perucco, B. J. Caldarone, R. Flavell, M. R. Picciotto, T. A. Ryan, O. Cremona, and P. De Camilli. 2002. Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33:789-804. [DOI] [PubMed] [Google Scholar]
  12. [13]DuHadaway, J. B., W. Du, P. S. Donover, J. Baker, A. Liu, D. M. Sharp, A. J. Muller, and G. C. Prendergast. Transformation selective apoptosis triggered by farnesyltransferase inhibitors requires Bin1. Oncogene, in press. [DOI] [PubMed]
  13. [14]DuHadaway, J. B., F. J. Lynch, S. Brisbay, C. Bueso-Ramos, P. Troncoso, T. McDonnell, and G. C. Prendergast. 2003. Immunohistochemical analysis of Bin1/Amphiphysin II in human tissues: diverse sites of nuclear expression and losses in prostate cancer. J. Cell. Biochem. 88:635-642. [DOI] [PubMed] [Google Scholar]
  14. [15]DuHadaway, J. B., D. Sakamuro, D. L. Ewert, and G. C. Prendergast. 2001. Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res. 61:3151-3156. [PubMed] [Google Scholar]
  15. [16]Elliott, K., K. Ge, W. Du, and G. C. Prendergast. 2000. The c-Myc-interacting adaptor protein Bin1 activates a caspase-independent cell death program. Oncogene 19:4669-4684. [DOI] [PubMed] [Google Scholar]
  16. [17]Elliott, K., D. Sakamuro, A. Basu, W. Du, W. Wunner, P. Staller, S. Gaubatz, H. Zhang, E. Prochownik, M. Eilers, and G. C. Prendergast. 1999. Bin1 functionally interacts with Myc and inhibits cell proliferation via multiple mechanisms. Oncogene 18:3564-3573. [DOI] [PubMed] [Google Scholar]
  17. [18]Farsad, K., N. Ringstad, K. Takei, S. R. Floyd, K. Rose, and P. De Camilli. 2001. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155:193-200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. [19]Gallily, R., and N. Savion. 1983. Cultivation, proliferation and characterization of thymic macrophages. Immunology 50:139-148. [PMC free article] [PubMed] [Google Scholar]
  19. [20]Ge, K., and G. C. Prendergast. 2000. Bin2, a functionally nonredundant member of the BAR adaptor gene family. Genomics 67:210-220. [DOI] [PubMed] [Google Scholar]
  20. [21]Gold, E. S., N. S. Morrissette, D. M. Underhill, J. Guo, M. Bassetti, and A. Aderem. 2000. Amphiphysin IIm, a novel amphiphysin II isoform, is required for macrophage phagocytosis. Immunity 12:285-292. [DOI] [PubMed] [Google Scholar]
  21. [22]Hogarty, M. D., X. Liu, P. M. Thompson, P. S. White, E. P. Sulman, J. M. Maris, and G. M. Brodeur. 2000. BIN1 inhibits colony formation and induces apoptosis in neuroblastoma cell lines with MYCN amplification. Med. Pediatr. Oncol. 35:559-562. [DOI] [PubMed] [Google Scholar]
  22. [23]Huang, D., G. Patrick, J. Moffat, L. H. Tsai, and B. Andrews. 1999. Mammalian Cdk5 is a functional homologue of the budding yeast Pho85 cyclin-dependent protein kinase. Proc. Natl. Acad. Sci. USA 96:14445-14450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. [24]Jackson, T., M. F. Allard, C. M. Sreenan, L. K. Doss, S. P. Bishop, and J. L. Swain. 1990. The c-myc proto-oncogene regulates cardiac development in transgenic mice. Mol. Cell. Biol. 10:3709-3716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. [25]Jackson, T., M. F. Allard, C. M. Sreenan, L. K. Doss, S. P. Bishop, and J. L. Swain. 1991. Transgenic animals as a tool for studying the effect of the c-myc proto-oncogene on cardiac development. Mol. Cell. Biochem. 104:15-19. [DOI] [PubMed] [Google Scholar]
  25. [26]Kadlec, L., and A. M. Pendergast. 1997. The amphiphysin-like protein 1 (ALP1) interacts functionally with the cABL tyrosine kinase and may play a role in cytoskeletal regulation. Proc. Natl. Acad. Sci. USA 94:12390-12395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. [27]Le, Q., R. Daniel, S. W. Chung, A. D. Kang, T. K. Eisenstein, B. M. Sultzer, H. Simpkins, and P. M. Wong. 1998. Involvement of C-Abl tyrosine kinase in lipopolysaccharide-induced macrophage activation. J. Immunol. 160:3330-3336. [PubMed] [Google Scholar]
  27. [28]Lee, E., M. Marcucci, L. Daniell, M. Pypaert, O. A. Weisz, G. C. Ochoa, K. Farsad, M. R. Wenk, and P. De Camilli. 2002. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193-1196. [DOI] [PubMed] [Google Scholar]
  28. [29]Lee, J., K. Colwill, V. Aneliunas, C. Tennyson, L. Moore, Y. Ho, and B. Andrews. 1998. Interaction of yeast Rvs167 and Pho85 cyclin-dependent kinase complexes may link the cell cycle to the actin cytoskeleton. Curr. Biol. 8:1310-1321. [DOI] [PubMed] [Google Scholar]
  29. [30]Leprince, C., F. Romero, D. Cussac, B. Vayssiere, R. Berger, A. Tavitian, and J. H. Camonis. 1997. A new member of the amphiphysin family connecting endocytosis and signal transduction pathways. J. Biol. Chem. 272:15101-15105. [DOI] [PubMed] [Google Scholar]
  30. [31]Li, F. Q., A. Coonrod, and M. Horwitz. 2000. Selection of a dominant negative retinoblastoma protein (RB) inhibiting satellite myoblast differentiation implies an indirect interaction between MyoD and RB. Mol. Cell. Biol. 20:5129-5139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [32]Lichte, B., R. Veh, H. Meyer, and M. Kilimann. 1992. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J. 11:2521-2530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. [33]Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evan. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686-1690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. [34]Mao, N. C., E. Steingrimsson, J. DuHadaway, W. Wasserman, J. C. Ruiz, N. G. Copeland, N. A. Jenkins, and G. C. Prendergast. 1999. The murine Bin1 gene functions early in myogenesis and defines a new region of synteny between mouse chromosome 18 and human chromosome 2. Genomics 56:51-58. [DOI] [PubMed] [Google Scholar]
  34. [35]McMahon, H. T., P. Wigge, and C. Smith. 1997. Clathrin interacts specifically with amphiphysin and is displaced by dynamin. FEBS Lett. 413:319-322. [DOI] [PubMed] [Google Scholar]
  35. [36]McPherson, P. S., E. P. Garcia, V. I. Slepnev, C. David, X. Zhang, D. Grabs, W. S. Sossin, R. Bauerfeind, Y. Nemoto, and P. De Camilli. 1996. A presynaptic inositol-5-phosphatase. Nature 379:353-357. [DOI] [PubMed] [Google Scholar]
  36. [37]Moens, C. B., B. R. Stanton, L. F. Parada, and J. Rossant. 1993. Defects in heart and lung development in compound heterozygotes for two different targeted mutations at the N-myc locus. Development 119:485-499. [DOI] [PubMed] [Google Scholar]
  37. [38]Muller, A. J., J. C. Young, A. M. Pendergast, M. Pondel, N. R. Landau, D. R. Littman, and O. N. Witte. 1991. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11:1785-1792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. [39]Munn, A. L., B. J. Stevenson, M. I. Geli, and H. Riezman. 1995. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6:1721-1742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. [40]Owen, D. J., P. Wigge, Y. Vallis, J. D. Moore, P. R. Evans, and H. T. McMahon. 1998. Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J. 17:5273-5285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. [41]Pear, W. S., G. P. Nolan, M. L. Scott, and D. Baltimore. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90:8392-8396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. [42]Ramjaun, A. R., and P. S. McPherson. 1998. Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J. Neurochem. 70:2369-2376. [DOI] [PubMed] [Google Scholar]
  42. [43]Ramjaun, A. R., K. D. Micheva, I. Bouchelet, and P. S. McPherson. 1997. Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J. Biol. Chem. 272:16700-16706. [DOI] [PubMed] [Google Scholar]
  43. [44]Ramjaun, A. R., J. Philie, E. de Heuvel, and P. S. McPherson. 1999. The N terminus of amphiphysin II mediates dimerization and plasma membrane targeting. J. Biol. Chem. 274:19785-19791. [DOI] [PubMed] [Google Scholar]
  44. [45]Razzaq, A., I. M. Robinson, H. T. McMahon, J. N. Skepper, Y. Su, A. C. Zelhof, A. P. Jackson, N. J. Gay, and C. J. O'Kane. 2001. Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev. 15:2967-2979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. [46]Razzaq, A., Y. Su, J. E. Mehren, K. Mizuguchi, A. P. Jackson, N. J. Gay, and C. J. O'Kane. 2000. Characterisation of the gene for Drosophila amphiphysin. Gene 241:167-174. [DOI] [PubMed] [Google Scholar]
  46. [47]Routhier, E. L., T. C. Burn, I. Abbaszade, M. Summers, C. F. Albright, and G. C. Prendergast. 2001. Human BIN3 complements the F-actin localization defects caused by loss of Hob3p, the fission yeast homolog of Rvs161p. J. Biol. Chem. 276:21670-21677. [DOI] [PubMed] [Google Scholar]
  47. [48]Routhier, E. L., P. S. Donover, and G. C. Prendergast. 2003. hob1+, the fission yeast homolog of Bin1, is dispensable for endocytosis or actin organization, but required for the response to starvation or genotoxic stress. Oncogene 22:637-648. [DOI] [PubMed] [Google Scholar]
  48. [49]Sakamuro, D., K. J. Elliott, R. Wechsler-Reya, and G. C. Prendergast. 1996. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat. Genet. 14:69-77. [DOI] [PubMed] [Google Scholar]
  49. [50]Shupliakov, O., P. Low, D. Grabs, H. Gad, H. Chen, C. David, K. Takei, P. De Camilli, and L. Brodin. 1997. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259-263. [DOI] [PubMed] [Google Scholar]
  50. [51]Simpson, F., N. K. Hussain, B. Qualmann, R. B. Kelly, B. K. Kay, P. S. McPherson, and S. L. Schmid. 1999. SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat. Cell. Biol. 1:119-124. [DOI] [PubMed] [Google Scholar]
  51. [52]Sivadon, P., F. Bauer, M. Aigle, and M. Crouzet. 1995. Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin. Mol. Gen. Genet. 246:485-495. [DOI] [PubMed] [Google Scholar]
  52. [53]Slepnev, V. I., G. C. Ochoa, M. H. Butler, and P. De Camilli. 2000. Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function by amphiphysin fragments comprising these sites. J. Biol. Chem. 275:17583-17589. [DOI] [PubMed] [Google Scholar]
  53. [54]Slepnev, V. I., G. C. Ochoa, M. H. Butler, D. Grabs, and P. D. Camilli. 1998. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281:821-824. [DOI] [PubMed] [Google Scholar]
  54. [55]Sparks, A. B., N. G. Hoffman, S. J. McConnell, D. M. Fowlkes, and B. K. Kay. 1996. Cloning of ligand targets: systematic isolation of SH3 domain-containing proteins. Nat. Biotech. 14:741-744. [DOI] [PubMed] [Google Scholar]
  55. [56]Takei, K., V. I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39. [DOI] [PubMed] [Google Scholar]
  56. [57]Todaro, G. J., and H. Green. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. [58]Tsutsui, K., Y. Maeda, K. Tsutsui, S. Seki, and A. Tokunaga. 1997. cDNA cloning of a novel amphiphysin isoform and tissue-specific expression of its multiple splice variants. Biochem. Biophys. Res. Commun. 236:178-183. [DOI] [PubMed] [Google Scholar]
  58. [59]Wechsler-Reya, R., K. Elliott, M. Herlyn, and G. C. Prendergast. 1997. The putative tumor suppressor BIN1 is a short-lived nuclear phosphoprotein, the localization of which is altered in malignant cells. Cancer Res. 57:3258-3263. [PubMed] [Google Scholar]
  59. [60]Wechsler-Reya, R., D. Sakamuro, J. Zhang, J. Duhadaway, and G. C. Prendergast. 1997. Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J. Biol. Chem. 272:31453-31458. [DOI] [PubMed] [Google Scholar]
  60. [61]Wechsler-Reya, R. J., K. J. Elliott, and G. C. Prendergast. 1998. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol. Cell. Biol. 18:566-575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. [62]Wigge, P., K. Kohler, Y. Vallis, C. A. Doyle, D. Owen, S. P. Hunt, and H. T. McMahon. 1997. Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell 8:2003-2015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. [63]Wigge, P., Y. Vallis, and H. T. McMahon. 1997. Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr. Biol. 7:554-560. [DOI] [PubMed] [Google Scholar]
  63. [64]Zelhof, A. C., H. Bao, R. W. Hardy, A. Razzaq, B. Zhang, and C. Q. Doe. 2001. Drosophila amphiphysin is implicated in protein localization and membrane morphogenesis but not in synaptic vesicle endocytosis. Development 128:5005-5015. [DOI] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Muller, A. J., Baker, J. F., DuHadaway, J. B., Ge, K., Farmer, G., Donover, P. S., Meade, R., Reid, C., Grzanna, R., Roach, A. H., Shah, N., Soler, A. P., & Prendergast, G. C.
Affiliations
  • DuPont (United States) (US)
  • The Wistar Institute (US)
  • University of Pennsylvania (US)
  • Lankenau Institute for Medical Research (US)
Corresponding author
Prendergast, George C.
ORCID
Venue
Molecular and Cellular Biology
Publisher
Informa UK Limited
Published
2003-06-01
Volume
23
Issue
12
Pages
4295-4306
ISSN
  • 0270-7306 (ISSN-L)
  • 1098-5549
DOI
10.1128/mcb.23.12.4295-4306.2003
PMC
PMC156129
OpenAlex
W2108808803
Cited by
139
References
1
Citations by year
2026: 4 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 14 · 2021: 14 · 2020: 9 · 2019: 4 · 2018: 3 · 2017: 4 · 2016: 7 · 2015: 6 · 2014: 7 · 2013: 7 · 2012: 7
FWCI
1.27
Type
journal article
Language
en
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Molecular and Cellular Biology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
DuPont
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiomyopathy and Myosin Studies
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Keywords
BIN1, gene knockout, myofibril formation, endocytosis, phagocytosis, actin cytoskeleton, alternative splicing, cardiac muscle development, perinatal lethality, mouse embryonic fibroblasts, macrophages
MeSH terms
Actins, Animals, Carrier Proteins, Cell Division, Cell Line, Cytoskeleton, Endocytosis, Fibroblasts, Immunohistochemistry, Macrophages, Models, Genetic, Muscles, Cardiomyopathies, Nerve Tissue Proteins, Nuclear Proteins, Phagocytosis, Time Factors, Blotting, Western, Polymerase Chain Reaction, Mutagenesis, Site-Directed, Culture Media, Serum-Free, Apoptosis, Protein Structure, Tertiary, Muscle, Skeletal, Protein Isoforms, Tumor Suppressor Proteins, Adaptor Proteins, Signal Transducing, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review