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Cytoskeletal Competence Requires Protein Chaperones

  • Roy Quinlan
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 28)

Abstract

The cytoskeleton is the internal structure of the cell that makes diverse cellular functions possible. These structures are extremely dynamic, undergoing continual remodelling within the cytoplasm and requiring continual change in the protein-protein interactions as part of their function. It is therefore not surprising that cytoskeletal proteins require the attention of protein chaperones at all stages of their life. Initially, chaperonins ensure the nascent chains of actin and tubulin fold correctly as they emerge from the ribosome and in this review, the role of the small heat shock proteins (sHSPs) in further cytoskeletal function will be discussed. Chaperones are most certainly important components in the birth and life of the cytoskeleton.

Keywords

Glial Fibrillary Acid Protein Intermediate Filament Small Heat Shock Protein Actin Assembly Intermediate Filament Network 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Altamirano MM, Golbik R, Zahn R, Buckle AM, Fersht AR (1997) Refolding chromatography with immobilized mini-chaperones. Proc Natl Acad Sci USA 94:3576–3578PubMedCrossRefGoogle Scholar
  2. Arai H, Atomi Y (1997) Chaperone activity of alpha B-crystallin suppresses tubulin aggregation through complex formation. Cell Struct Funct 22:539–544PubMedCrossRefGoogle Scholar
  3. Barbato R, Menabo R, Dainese P, Carafoli E, Schiaffino S, Di Lisa F (1996) Binding of cytosolic proteins to myofibrils in ischemic rat hearts. Circ Res 78:821–828PubMedCrossRefGoogle Scholar
  4. Bennardini F, Wrzosek A, Chiesi M (1992) Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ Res 71:288–294PubMedCrossRefGoogle Scholar
  5. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behl J, Lutsch G (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269:20780–20784PubMedGoogle Scholar
  6. Bershadsky A, Chausovsky A, Becker E, Lyubimova A, Geiger B (1996) Involvement of microtubules in the control of adhesion-dependent signal-transduction. Curr Biol 6:1279–1289PubMedCrossRefGoogle Scholar
  7. Bhat SP, Hale IL, Matsumoto B, Elghanayan D (1999) Ectopic expression of alpha B-crystallin in Chinese hamster ovary cells suggests a nuclear role for this protein. Eur J Cell Biol 78:143–150PubMedCrossRefGoogle Scholar
  8. Bluhm WF, Martin JL, Mestril R, Dillmann WH (1998) Specific heat shock proteins protect microtubules during simulated ischemia in cardiac myocytes. Am Physiol 275:H2243–H2249Google Scholar
  9. Bova MP, Yaron O, Huang Q, Ding L, Haley DA, Stewart PL, Horwitz J (1999) Mutation R120G in alphαB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function [In Process Citation]. Proc Natl Acad Sei USA 96:6137–6142CrossRefGoogle Scholar
  10. Brophy CM, Dickinson M, Woodrum D (1999a) Phosphorylation of the small heat shock-related protein, HSP20, in vascular smooth muscles is associated with changes in the macromolecular associations of HSP20. J Biol Chem 274:6324–6329PubMedCrossRefGoogle Scholar
  11. Brophy CM, Lamb S, Graham A (1999b) The small heat shock-related protein-20 is an actinassociated protein. J Vasc Surg 29:326–333PubMedCrossRefGoogle Scholar
  12. Chiesi M, Longoni S, Limbruno U (1990) Cardiac alpha-crystallin. III. Involvement during heart ischemia. Mol Cell Biochem 97:129–136PubMedCrossRefGoogle Scholar
  13. Correia I, Chu D, Chou YH, Goldman RD, Matsudaira P (1999) Integrating the actin and vimentin cytoskeletons. adhesion-dependent formation of fibrin-vimentin complexes in macrophages. J Cell Biol 146:831–842PubMedCrossRefGoogle Scholar
  14. Czar MJ, Welsh MJ, Pratt WB (1996) Immunofluorescence localization of the 90-kDa heat-shock protein to cytoskeleton. Eur J Cell Biol 70:322–330PubMedGoogle Scholar
  15. De Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int J Biol Macromol 22:151–162PubMedCrossRefGoogle Scholar
  16. Djabali K, deNechaud B, Landon F, Portier MM (1997) Alpha B-crystallin interacts with intermediate filaments in response to stress. J Cell Sci 110:2759–2769PubMedGoogle Scholar
  17. Duguid JR, Rohwer RG, Seed B (1988) Isolation of cDNAs of scrapie-modulated RNAs by subtractive hybridization of a cDNA library. Proc Natl Acad Sei USA 85:5738–5742CrossRefGoogle Scholar
  18. Ehrnsperger M, Graber S, Gaestel M, Buchner J (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 16: 221–229PubMedCrossRefGoogle Scholar
  19. Goebel HH, Bornemann A (1993) Desmin pathology in neuromuscular diseases. Virchows Arch B Cell Pathol Incl Mol Pathol 64:127–135PubMedCrossRefGoogle Scholar
  20. Goldfarb LG, Park KY, Cervenakova L, Gorokhova S, Lee HS, Vasconcelos O, Nagle JW, Semino-Mora C, Sivakumar K, Dalakas MC (1998) Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat Genet 19:402–403PubMedCrossRefGoogle Scholar
  21. Goldman JE, Corbin E (1988) Isolation of a major protein component of Rosenthal fibers. Am J Pathol 130:569–578PubMedGoogle Scholar
  22. Golenhofen N, Ness W, Koob R, Htun P, Schaper W, Drenckhahn D (1998) Ischemia-induced phosphorylation and translocation of stress protein alpha B-crystallin to Z lines of myocardium. Am J Physiol 274:H1457–H1464PubMedGoogle Scholar
  23. Golenhofen N, Htun P, Ness W, Koob R, Schaper W, Drenckhahn D (1999) Binding of the stress protein alpha B-crystallin to cardiac myofibrils correlates with the degree of myocardial damage during ischemia/reperfusion in vivo. J Mol Cell Cardiol 31:569–580PubMedCrossRefGoogle Scholar
  24. Gopalakrishnan S, Takemoto L (1992) Binding of actin to lens alpha crystallins. Curr Eye Res 11: 929–933PubMedCrossRefGoogle Scholar
  25. Guay J, Lambert H, GingrasBreton G, Lavoie JN, Huot J, Landry J (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110:357–368PubMedGoogle Scholar
  26. Herrmann H, Aebi U (2000) Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12:79–90PubMedCrossRefGoogle Scholar
  27. Hirose M, Ishizaki T, Watanabe N, Uehata M, Kranenburg O, Moolenaar WH, Matsumura F, Maekawa M, Bito H, Narumiya S (1998) Molecular dissection of the Rho-associated protein kinase (pl60ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141:1625–1636PubMedCrossRefGoogle Scholar
  28. Hoover HE, Thuerauf DJ, Martindale JJ, Glembotski CC (2000) Alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alpha B-crystallin as a target of the p38 branch of the cardiac stress response. J Biol Chem 275:23825–23833PubMedCrossRefGoogle Scholar
  29. Huot J, Roy G, Lambert H, Chretien P, Landry J (1991) Increased survival after treatments with anticancer agents of Chinese-hamster cells expressing the human mr 27,000 heat-shock protein. Cancer Res 51:5245–5252PubMedGoogle Scholar
  30. Huot J, Houle F, Marceau F, Landry J (1997) Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80:383–392PubMedCrossRefGoogle Scholar
  31. Huot J, Houle F, Rousseau S, Deschesnes RG, Shah GM, Landry J (1998) SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J Cell Biol 143:1361–1373PubMedCrossRefGoogle Scholar
  32. Ito H, Okamoto K, Nakayama H, Isobe T, Kato K (1997) Phosphorylation of alpha B-crystallin in response to various types of stress. J Biol Chem 272:29934–29941PubMedCrossRefGoogle Scholar
  33. Iwaki T, Kume-Iwaki A, Liem RKH, Goldman JE (1989) αB-crystallin is expressed in nonlenticular tissues and accumulates in Alexander’s disease brain. Cell 57:71–78PubMedCrossRefGoogle Scholar
  34. Iwaki T, Iwaki A, Tateishi J, Sakaki Y, Goldman JE (1993) Alpha-b-crystallin and 27-kd heat-shock protein are regulated by stress conditions in the central-nervous-system and accumulate in Rosenthal fibers. Am J Pathol 143:487–495PubMedGoogle Scholar
  35. Jakobs PM, Hess JF, FitzGerald PG, Kramer P, Weleber RG, Litt M (2000) Autosomal-dominant congenital cataract associated with a deletio n mutation in the human beaded filament protein gene bFSP2. Am J Hum Genet 66:1432–1436PubMedCrossRefGoogle Scholar
  36. Kasi VS, Kuppuswamy D (1999) Inhibition of src family kinases by a combinatorial action of 5’-AMP and small heat shock proteins, identified from the adult heart. Mol Cell Biol 19:6858–6871PubMedGoogle Scholar
  37. Kato K, Ito H, Kamei K, Inaguma Y, Iwamoto I, Saga S (1998) Phosphorylation of alphαB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J Biol Chem 273:28346–28354PubMedCrossRefGoogle Scholar
  38. Kato S, Hirano A, Umahara T, Llena JF, Herz F, Ohama E (1992) Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of alpha B-crystallin, ubiquitin and stress-response protein 27. Acta Neuropathol Berl 84:443–448PubMedGoogle Scholar
  39. Kaukinen KH, Tranbarger TJ, Misra S (1996) Post-termination-induced and hormonally dependent expression of low-molecular-weight heat shock protein genes in Douglas fir. Plant Mol Biol 30:1115–1128PubMedCrossRefGoogle Scholar
  40. Kaverina I, Rottner K, Small JV (1998) Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 142:181–190PubMedCrossRefGoogle Scholar
  41. Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394: 595–599PubMedCrossRefGoogle Scholar
  42. Konishi H, Matsuzaki H, Tanaka M, Takemura Y, Kuroda S, Ono Y, Kikkawa U (1997) Activation of protein kinase B (Akt/RAC-protein kinase) by cellular stress and its association with heat shock protein Hsp27. FEBS Lett 410:493–498PubMedCrossRefGoogle Scholar
  43. Kosako H, Goto H, Yanagida M, Matsuzawa K, Fujita M, Tomono Y, Okigaki T, Odai H, Kaibuchi K, Inagaki M (1999) Specific accumulation of Rho-associated kinase at the cleavage furrow during cytokinesis: cleavage furrow-specific phosphorylation of intermediate filaments [In Process Citation]. Oncogene 18:2783–2788PubMedCrossRefGoogle Scholar
  44. Koyama Y, Goldman JE (1999) Formation of GFAP cytoplasmic inclusions in astrocytes and their disaggregation by alphαB-crystallin [In Process Citation]. Am J Pathol 154:1563–1572PubMedCrossRefGoogle Scholar
  45. Krief S, Faivre JF, Robert P, Le Douarin B, Brument-Larignon N, Lefrere I, Bouzyk MM, Anderson KM, Greller LD, Tobin FL et al. (1999) Identification and characterization of cvHsp. A novel human small stress protein selectively expressed in cardiovascular and insulin-sensitive tissues. J Biol Chem 274:36592–36600PubMedCrossRefGoogle Scholar
  46. Landry J, Huot J (1999) Regulation of actin dynamics by stress-activated protein kinase 2 (SAPK2)-dependent phosphorylation of heat-shock protein of 27kDa (Hsp27). Biochem Soc Symp 64:79–89PubMedGoogle Scholar
  47. Landry J, Chretien P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol 109:7–15PubMedCrossRefGoogle Scholar
  48. Lavoie JN, Gingras Breton G, Tanguay RM, Landry J (1993a) Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization J Biol Chem 268:3420–3429Google Scholar
  49. Lavoie JN, Hickey E, Weber LA, Landry J (1993b) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268: 24210–24214PubMedGoogle Scholar
  50. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15:505–516PubMedGoogle Scholar
  51. Li D, Tapscoft T, Gonzalez O, Burch PE, Quinones MA, Zoghbi WA, Hill R, Bachinski LL, Mann DL, Roberts R (1999) Desmin mutation responsible for idiopathic dilated cardiomyopathy. Circulation 100:461–464PubMedCrossRefGoogle Scholar
  52. Liao J, Lowthert LA, Ghori N, Omary MB (1995) The 70-kDa heat shock proteins associate with glandular intermediate filaments in an ATP-dependent manner. J Biol Chem 270:915–922PubMedCrossRefGoogle Scholar
  53. Litt M, Kramer P, LaMorticella DM, Murphey W, Lovrien EW, Weleber RG (1998) Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum Mol Genet 7:471–474PubMedCrossRefGoogle Scholar
  54. Loktionova SA, Kabakov AE (1998) Protein phosphatase inhibitors and heat preconditioning prevent Hsp27 dephosphorylation, F-actin disruption and deterioration of morphology in ATP-depleted endothelial cells. FEBS Lett 433:294–300PubMedCrossRefGoogle Scholar
  55. Longoni S, Lattonen S, Bullock G, Chiesi M (1990) Cardiac alpha-crystallin. II. Intracellular localization. Mol Cell Biochem 97:121–128PubMedCrossRefGoogle Scholar
  56. Lowe J, Errington DR, Lennox G, Pike I, Spendlove I, Landon M, Mayer RJ (1992) Ballooned neurons in several neurodegenerative diseases and stroke contain alpha B crystallin. Neuropathol Appl Neurobiol 18:341–350PubMedCrossRefGoogle Scholar
  57. Madaule P, Eda M, Watanabe N, Fujisawa K, Matsuoka T, Bito H, Ishizaki T, Narumiya S (1998) Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature 394:491–494PubMedCrossRefGoogle Scholar
  58. Miron T, Wilchek M, Geiger B (1988) Characterization of an inhibitor of actin polymerization in vinculin-rich fraction of turkey gizzard smooth-muscle. Eur J Biochem 178:543–553PubMedCrossRefGoogle Scholar
  59. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B (1991) A 25-kd inhibitor of actin polymerization is a low-molecular mass heat-shock protein. J Cell Biol 114:255–261PubMedCrossRefGoogle Scholar
  60. Mizzen LA, Welch WJ (1988) Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J Cell Biol 106: 1105–1116PubMedCrossRefGoogle Scholar
  61. Muchowski PJ, Hays LG, Yates III JR, Clark JI (1999a) ATP and the core’ alpha-crystallin’ domain of the small heat shock protein alphαB-crystallin. J Biol Chem (submitted)Google Scholar
  62. Muchowski PJ, Valdez MM, Clark JI (1999b) αB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest Ophthalmol Vis Sei 40:951–958Google Scholar
  63. Nicholl ID, Quinlan RA (1994) Chaperone activity of N-crystallins modulates intermediate filament assembly. EMBO J 13:945–953PubMedGoogle Scholar
  64. Olinkcoux M, Arcangeletti C, Pinardi F, Minisini R, Huesca M, Chezzi C, Scherrer K (1994) Cytolocation of prosome antigens on intermediate filament subnetworks of cytokeratin, vimentin and desmin type. J Cell Sci 107:353–366Google Scholar
  65. Perng MD, Cairns L, van den Ijssel P, Prescott A, Hutcheson AM, Quinlan RA (1999a) Intermediate filament interactions can be altered by HSP27 and ocB-crystallin. J Cell Sci 112:2099–2112PubMedGoogle Scholar
  66. Perng MD, Muchowski PJ, van den Ijssel P, Wu GJS, Clark JI, Quinlan RA (1999b) The cardiomyopathy and lens cataract mutation in αB-crystallin compromises secondary, tertiary and quaternary protein structure and reduces in vitro chaperone activity. J Biol Chem 274:33235–33243PubMedCrossRefGoogle Scholar
  67. Pietrowski D, Durante MJ, Liebstein A, Schmitt-John T, Werner T, Graw J (1994) Alpha-crystallins are involved in specific interactions with the murine gamma D/E/F-crystallin-encoding gene. Gene 144:171–178PubMedCrossRefGoogle Scholar
  68. Piotrowicz RS, Levin EG (1997) Basolateral membrane-associated 27-kDa heat shock protein and microfilament polymerization. J Biol Chem 272:25920–25927PubMedCrossRefGoogle Scholar
  69. Prahlad V, Yoon M, Moir RD, Vale RD, Goldman RD (1998) Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J Cell Biol 143:159–170PubMedCrossRefGoogle Scholar
  70. Rembold CM, Foster DB, Strauss JD, Wingard CJ, Eyk JE (2000) cGMP-mediated phosphorylation of heat shock protein 20 may cause smooth muscle relaxation without myosin light chain dephosphorylation in swine carotid artery. J Physiol (Lond) 524 Pt 3:865–878CrossRefGoogle Scholar
  71. Rousseau S, Houle F, Kotanides H, Witte L, Waltenberger J, Landry J, Huot J (2000) Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J Biol Chem 275:10661–10672PubMedCrossRefGoogle Scholar
  72. Shama KM, Suzuki A, Harada K, Fujitani N, Kimura H, Ohno S, Yoshida K (1999) Transient up-regulation of myotonic dystrophy protein kinase-binding protein, MKBP, and HSP27 in the neonatal myocardium. Cell Struct Funct 24:1–4PubMedCrossRefGoogle Scholar
  73. Shroff NP, Cherian-Shaw M, Bera S, Abraham EC (2000) Mutation of R116C results in highly oligomerized alpha A-crystallin with modified structure and defective chaperone-like function. Biochemistry 39:1420–1426PubMedCrossRefGoogle Scholar
  74. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M (1992) Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett 313:307–313PubMedCrossRefGoogle Scholar
  75. Sugiyama Y, Suzuki A, Kishikawa M, Akutsu R, Hirose T, Waye MM, Tsui SK, Yoshida S, Ohno S, Sanjay TW (2000) Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation. J Biol Chem 275:1095–1104PubMedCrossRefGoogle Scholar
  76. Suzuki A, Sugiyama Y, Hayashi Y, Nyu-i N, Yoshida M, Nonaka I, Ishiura S, Arahata K, Ohno S, Sanjay TW (1998) MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase. J Cell Biol 140:1113–1124PubMedCrossRefGoogle Scholar
  77. Thomas GP, Welch WJ, Matthews MB, Feramisco JR (1982) Molecular and cellular effects of heatshock and related treatments on mammalian tissue-culture cells. Cold Spring Harbor Symp Quant Biol 46:985–996PubMedCrossRefGoogle Scholar
  78. Van de Klundert FAJ M, Gijsen MLJ, van den Ijssel PRLA, Snoeckx LHEH, de Jong WW (1998) Alpha B-crystallin and hsp25 in neonatal cardiac cells—differences in cellular localization under stress conditions. Eur J Cell Biol 75:38–45CrossRefGoogle Scholar
  79. Van den Ijssel P, Norman DG, Quinlan RA (1999) Small heat shock proteins in the limelight [In Process Citation]. Curr Biol 9:R103–R105PubMedCrossRefGoogle Scholar
  80. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, Chateau D, Chapon F, Tome F, Dupret JM et al. (1998) A missense mutation in the alphαB-crystallin chaperone gene causes a desminrelated myopathy. Nat Genet 20:92–95PubMedCrossRefGoogle Scholar
  81. Wang K, Spector A (1996) a-crystallin stabilises actin filaments and prevents cytochalasininduced depolymerisation in a phosphorylation-dependent manner. Eur J Biochem 242: 56–66PubMedCrossRefGoogle Scholar
  82. Waterman-Storer CM, Worthylake RA, Liu BP, Burridge K, Salmon ED (1999) Microtubule growth activates Racl to promote lamellipodial protrusion in fibroblasts [see comments]. Nat Cell Biol 1:45–50PubMedCrossRefGoogle Scholar
  83. Waterman-Storer CM, Salmon WC, Salmon ED (2000) Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells. Mol Biol Cell 11:2471–2483PubMedGoogle Scholar
  84. Welch WJ, Feramisco JR (1985) Disruption of the three cytoskeletal networks in mammalian cells does not affect transcription, translation, or protein translocation changes induced by heat shock. Mol Cell Biol 5:1571–1581PubMedGoogle Scholar
  85. Welch WJ, Mizzen LA (1988) Characterization of the thermotolerant cell. II. Effects on the intracellular distribution of heat-shock protein 70, intermediate filaments, and small nuclear ribonucleoprotein complexes. J Cell Biol 106:974–981CrossRefGoogle Scholar
  86. Welch WJ, Feramisco JR, Blose SH (1985) The mammalian stress response and the cytoskeleton: alterations in intermediate filaments. Ann NY Acad Sci 455:57–67PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Roy Quinlan
    • 1
  1. 1.Department of Biological SciencesDurhamUK

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